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First published online September 3, 2008; 10.1104/pp.108.123026 Plant Physiology 148:1570-1582 (2008) © 2008 American Society of Plant Biologists OPEN ACCESS ARTICLE
β-Subunits of the SnRK1 Complexes Share a Common Ancestral Function Together with Expression and Function Specificities; Physical Interaction with Nitrate Reductase Specifically Occurs via AKINβ1-Subunit1,[C],[OA]Laboratoire Signalisation et Régulation Coordonnée du Métabolisme Carboné et Azoté, Institut de Biotechnologie des Plantes (UMR8618), Université Paris-Sud, F–91405 Orsay cedex, France
The SNF1/AMPK/SnRK1 kinases are evolutionary conserved kinases involved in yeast, mammals, and plants in the control of energy balance. These heterotrimeric enzymes are composed of one  -type catalytic subunit and two  - and β-type regulatory subunits. In yeast it has been proposed that the β-type subunits regulate both the localization of the kinase complexes within the cell and the interaction of the kinases with their targets. In this work, we demonstrate that the three β-type subunits of Arabidopsis (Arabidopsis thaliana; AKINβ1, AKINβ2, and AKINβ3) restore the growth phenotype of the yeast sip1 sip2gal83 triple mutant, thus suggesting the conservation of an ancestral function. Expression analyses, using AKINβ promoter::β-glucuronidase transgenic lines, reveal different and specific patterns of expression for each subunit according to organs, developmental stages, and environmental conditions. Finally, our results show that the β-type subunits are involved in the specificity of interaction of the kinase with the cytosolic nitrate reductase. Together with previous cell-free phosphorylation data, they strongly support the proposal that nitrate reductase is a real target of SnRK1 in the physiological context. Altogether our data suggest the conservation of ancestral basic function(s) together with specialized functions for each β-type subunit in plants.
The SNF1/AMPK kinase family plays an important role in the control of the energy balance. In yeast, SNF1 (for Suc nonfermenting 1) is as a key player in the shift from fermentative to oxidative metabolism in response to Glc deprivation (diauxic shift; Hardie et al., 1998  ). Indeed, a quarter of the genome presents a SNF1-dependent change in expression during this shift (Young et al., 2003). In mammals, AMPK, the SNF1 homolog, has been involved in sensing the cellular and whole-body energy levels. At the cellular level, this kinase, once activated by an increase in AMP level, switches off ATP-consuming pathways such as fatty acid, cholesterol, and protein syntheses, and switches on ATP-producing pathways such as fatty acid oxidation and glycolysis (Hardie, 2004). At the whole-body level, AMPK is activated in response to muscle contraction, resulting in an increased fatty acid oxidation and Glc uptake (Hardie and Carling, 1997; Merrill et al., 1997; Fryer et al., 2002). This enzyme also plays an important role in Glc homeostasis since it participates in the inhibition of insulin production and secretion by the islet β cells when Glc level in blood is low (da Silva Xavier et al., 2000, 2003) and to the inhibition of Glc metabolism in liver (Foretz et al., 1998; Leclerc et al., 1998; for review, see Rutter et al., 2003). AMPK also regulates energy intake, its activation in hypothalamus leading to a stimulation of food intake (Andersson et al., 2004; Minokoshi et al., 2004). In plants, several reports have involved SnRK1 (for SNF1-related protein kinase 1) in the regulation of metabolic pathways (for review, see Polge and Thomas, 2007). Indeed, Suc-P synthase, nitrate reductase (NR), and TPS5 (for trehalose-P synthase 5) have been identified as in vitro phosphorylation targets of SnRK1 (Sugden et al., 1999; Harthill et al., 2006). SnRK1 kinases also regulate the expression of several genes involved in carbohydrate metabolism such as Suc synthase and -amylase (Purcell et al., 1998; Laurie et al., 2003) and is involved in the regulation of starch synthesis (Zhang et al., 2001; Geigenberger, 2003; Thelander et al., 2004). Recently a major contribution was brought by the work of Baena-González and collaborators using transient expression experiments and transgenic plants. Their data implicate the two Arabidopsis (Arabidopsis thaliana) SnRK1 kinases as central integrators of transcriptional networks in response to stress and energy signaling (Baena-González et al., 2007), thus reinforcing diverse previous reports (Nemeth et al., 1998; Farras et al., 2001; Bradford et al., 2003; Buitink et al., 2003; Hao et al., 2003; Thelander et al., 2004; Gissot et al., 2006; Radchuk et al., 2006).
In all eukaryotic kingdoms, SNF1/AMPK/SnRK1 kinases function as heterotrimeric complexes composed of one catalytic subunit, the
Concerning the β-type subunits, the conservation among the yeast, mammal, and plant SIP/AMPKβ/SnRKβ proteins spread along three regions, the ASC (for association with Snf1 complex), the KIS (for kinase-interacting sequence), and the GBD (for glycogen-binding domain) domain. In yeast, the ASC domain, located at the C terminus, allows the interaction of the β-subunits (SIP1, SIP2, GAL83) with SNF4 (Jiang and Carlson, 1997
Plant β-subunits can be grouped in two classes. One class of two plant β-subunits is composed of proteins presenting the characteristics of the three yeast and the two mammalian β-subunits in that they all have the three conserved domains previously described (Yang et al., 1992
Several studies have highlighted an emerging importance of the β-type subunits within the complex, making them particularly attractive. For instance, in plants, a 90% to 95% decrease in StubGAL83 expression, a potato (Solanum tuberosum) β-type subunit, leads to an abnormal development of roots and tubers (Lovas et al., 2003
Yeast SNF1, mammalian AMPK, and plant SnRK1 kinases are now considered as global metabolic regulators. To gain more insights into the role of plant SnRK1 complexes, we have focused our study on the three β-type subunits of Arabidopsis, AKINβ1, AKINβ2, and AKINβ3. We demonstrate that these three subunits restore the phenotype of the yeast sip1
AKINβ1, AKINβ2, and AKINβ3 Share a Common Ancestral Function(s)
To get insights into the function of the plant β-subunits, we have performed yeast functional complementation experiments using a yeast β-subunit triple mutant (Schmidt and McCartney, 2000
Analysis of AKINβ1, AKINβ2, and AKINβ3 Genes Reveals Different Potential Regulatory Elements To determine whether the three plant β-type subunits could have redundant functions, as suggested by the yeast functional complementation experiments described above, we have undertaken a detailed study of their promoter regions (Fig. 2 ).
The AKINβ1 promoter (772 bp from transcription start site) contains one 6-bp consensus sequence known as auxin response element (Ulmasov et al., 1997 ; Fig. 2). However, digital northern analysis carried out with Genevestigator (Zimmermann et al., 2004; https://www.genevestigator.ethz.ch) did not reveal any potential regulation by auxin. One pollen box is present (Twell et al., 1991), as well as two dark induction or light repression boxes (Dehesh et al., 1990; Inaba et al., 2000; Fig. 2). Two antagonistic types of boxes have also been found in this promoter, six sugar-repressive boxes (Lu et al., 1998; Morita et al., 1998) and one sugar-inducible box (Sun et al., 2003; Fig. 2).
In the AKINβ2 promoter (998 bp from transcription start site), a domain similar to the LAT56 pollen motif is present (Twell et al., 1991
The AKINβ3 promoter (976 bp from transcription start site) contains 17 pollen boxes (Fig. 2). Seven AAATGA boxes are on the major strand and three on the minus strand (Weterings et al., 1995 The detailed analysis of the promoters of the three AKINβ genes suggests a differential regulation of gene expression. To confirm this assessment in vivo, we have studied the expression patterns of the three genes in different organs, at different developmental stages, and in response to light conditions and to sugar availability.
To investigate expression patterns in different organs and at different developmental stages, we have produced AKINβ promoter::GUS transgenic lines. Translational fusions were made between the UIDA reporter gene and fragments of AKINβ1, AKINβ2, and AKINβ3 promoters corresponding, respectively, to 772, 998, and 976 bp upstream of the transcription start, and containing the subset of regulation motifs in these regions described in Figure 2. Staining data, shown in Figure 3 , are representative of the results obtained for at least three AKINβ1::GUS, AKINβ2::GUS, and AKINβ3::GUS stable homozygous transgenic lines.
GUS staining experiments indicate that there is at least one β-subunit expressed in all the organs and tissues analyzed (Fig. 3D). Some organs and tissues express the three AKIN::GUS constructs. This is found in the cotyledons soon after germination (data not shown) and in roots from 72-h-old seedlings (Fig. 3A, photographs b), in the primordia of roots and reproductive organs (Fig. 3B), in the stamen filament and the pistil of young buds, and in mature pollen (Fig. 3B, photographs f). These results suggest the existence of three types of SnRK1 complexes in these tissues, β1, β2, and β3 ( representing 1 or 2 and being or β). Interestingly there are also tissues where the expression of only one β-subunit is detected. AKINβ1 is mainly expressed in the sepals of young buds (Fig. 3B, photographs 1c and 1d) and in the ovary wall (Fig. 3B, photographs 1e and 1f). AKINβ2 is the main form in stigmata, in placenta with a strong coloration in septum (Fig. 3B, photographs e), in floral pedicel, and in the insertion area of the floral organs (Figs. 3B [photographs e] and 4A
). AKINβ3 is the main form in the root tip of 48-h-old seedlings (Fig. 3A, photograph 3a), in leaf primordia, in developing pollen, in ovules (Fig. 3C, photographs 3e and 3f), and in immature seeds (Fig. 3C, photograph 3g).
Altogether, the staining data showed that at least one β-subunit is expressed in each organ or tissue tested (Fig. 3D), suggesting a ubiquitous presence of the AKINβ-type proteins in the whole plant. Thus, these data also indirectly suggest the presence of AKIN kinase complexes in all the organs of Arabidopsis since we have previously shown that both the catalytic AKIN -subunit and AKINβ, one AKIN-subunit, appear constitutively expressed (Gissot et al., 2006). Another interesting result was the fact that in some organs the three β-type subunits present specific patterns of expression that moreover vary during organ development. It is noteworthy that, in opened flowers and siliques, there is nearly no overlap between the patterns of expression of the three β-type subunits (Fig. 3C).
During the analysis of AKINβ2-GUS expression pattern, a strong staining was detected in the pedicle during flower development (Fig. 4A). It is well known that in this region, after flowering, cells enter senescence to allow the abscission of floral parts. The increase of AKINβ2::GUS expression could be related to a program of cell death. The expression of AKIN genes during the process of senescence was thus followed by northern-blot experiments at different leaf developmental stages (named a–i), throughout the development of the plant (Fig. 4, B and C). Our results show that expression of all three β-type subunits is up-regulated at the advanced stages of senescence when most RNAs are degraded, as shown by hybridization with EF1
Regulatory sequences associated with dark induction have been identified in AKINβ1 and AKINβ3 promoters, reinforcing, for AKINβ1, previous data from our laboratory showing differential light regulation (Bouly et al., 1999
No significant variation of AKINβ2::GUS expression in response to darkness was detected using the experimental conditions described (Fig. 5B). For AKINβ3::GUS, GUS activity shows an average of 1.6- to 2.2-fold increase in gene expression after 2.5 d in the dark in two transformants (Fig. 4C). This result, together with the presence of a dark box in its promoter, suggests that AKINβ3 is transcriptionally regulated in these conditions. However, this dark box is different from the one present in the AKINβ1 promoter that was described as phytochrome dependent, suggesting that these two promoters could be dark regulated by different mechanisms. Since no variation was observed for AKINβ2, the observed differential expression effect is very likely linked to the AKINβ1 and AKINβ3 promoters.
The dark-induced variations of expression observed can be a direct consequence of dark/light conditions, as suggested by the presence of a dark-responsive element (phytochrome dependent) in the AKINβ1 promoter (Inaba et al., 2000
The same experiment has been performed with AKINβ3::GUS transgenic lines, but no significant variation was measured in the presence of Suc in our conditions (data not shown) nor reported in the Genevestigator database. These results suggest that, in contrast to AKINβ1, AKINβ3 gene expression is only regulated by a dark signal and is sugar independent. Altogether, these data suggest that expression of the AKINβ genes is related to the presence/absence of dark/sugar regulatory domains in their promoter sequences.
Since the β-type subunits of Arabidopsis present differential gene expression, we have hypothesized that they could interact specifically with different targets, as previously proposed in yeast (Vincent and Carlson, 1999
In Plants, the N-Terminal Variable Region of the β-Type Subunits May Confer the Specificity of Interaction with the Targets of the Kinase
Taking into account that sequence homology between AKINβ1 and AKINβ2 is mainly located in the C-terminal region of these proteins (GBD, KIS, and ASC domains), and since AKINβ2 was not able to interact with NR2, we suggested that the specificity of this interaction is dependent on the N-terminal region of the protein. Such a mechanism was also proposed by Vincent and Carlson (1999)
This article focuses on the study of the SnRK1 β-type subunits in Arabidopsis to attain a better understanding of the involvement of these subunits in the function(s) of the plant SNF1 kinases. This endeavor relies on the hypothesis proposed by Vincent and Carlson that the β-type subunits mediate the interaction between the kinase and its targets, imparting specific functions to the SNF1 kinase (Vincent and Carlson, 1999 ).
First, using GUS histochemical staining, we have shown that in all Arabidopsis organs tested, at least one β-type subunit is expressed. These data suggest a ubiquitous presence of AKINβ proteins and, thus, presumably of the AKIN complex in the whole plant since AKIN
We also show here that the dark/light-dependent variations in AKINβ1 (Bouly et al., 1999
We then wondered whether the Arabidopsis and yeast β-subunits have identical functions. In yeast, the three β-subunits have some redundant functions since only the complete deletion of the three β-subunits (sip1
Specific patterns of expression obtained for each AKINβ-subunit using GUS histochemical staining together with a differential regulation of gene expression led us to the hypothesis that each β-subunit could also have specific functions in relation with target binding and correct positioning for phosphorylation by the catalytic subunit of the complex. We thus examined the interaction between the AKINβ proteins and NR (NR2; Sugden et al., 1999 AKINβ1 and AKINβ2 present a high degree of identity, 49% in the whole protein, mainly located in the conserved C-terminal KIS and ASC domains (55%). Is the N-terminal region, the most divergent region, responsible for the differential interaction between AKINβ1 and AKINβ2 with NR2? To test this hypothesis, we have performed two-hybrid and cell-free binding experiments between NR2 and the different subdomains of each β-subunit. These experiments allowed us to show that, when deleted from its N-terminal region, AKINβ2 can interact with NR2 and that this interaction is mediated by the KIS and the ASC domains. Indeed, together or alone, these domains of AKINβ2 can interact with NR2, while in the presence of the N-terminal region no interaction was detected. Altogether, these data suggest that in the case of NR2, the N-terminal domain of the AKINβ1-subunit: (1) plays an important part in the specificity of interaction with the target; and (2) is not involved directly in the interaction itself. We can hypothesize that this variable region could allow the interaction only with specific targets and/or reinforce this interaction, thus being responsible for the functional consequences of specific SnRK1 complexes according to the β-subunit involved. In this case what could be the function of AKINβ3, the shorter plant-specific β-subunit lacking N-terminal and KIS-GBD regions? It could have a role of rescue, being able to interact with all the targets of the kinase, in a weaker way than the specific β-subunit. However, GUS histochemical experiments suggest a specific pattern of expression of this subunit within some tissues where AKINβ3 is the only β-type subunit detectable, suggesting that this enzyme subunit also has proper and specific functions. Moreover, two-hybrid screens performed in our laboratory using the three AKINβ-subunits as baits suggest that each β-subunit has a different set of partners (data not shown) and reinforces the hypothesis of distinct functions for the three β-type subunits in Arabidopsis. The results obtained in this study support the idea of a highly complex regulation of SnRK1 kinase complexes in plants with multiple combinations of subunits. The differential regulation of AKINβ gene expression according to developmental and environmental cues together with the specificity of interaction between AKINβ-subunits and the kinase targets provides a mechanism for this higher level of complexity. So, in a given situation (tissue, organ, environmental condition, or developmental stage), each β-subunit confers to the SnRK1 complex in which it is associated some unique substrate specificities resulting in divergent physiological consequences.
Plant Materials Arabidopsis (Arabidopsis thaliana) seeds, ecotype Columbia (C0), were grown in soil at 21°C under a 9-h-light/15-h-dark cycle (short day) or 16-h-light/8-h-dark cycle (long day). In vitro-cultured plants were germinated on half-strength Murashige and Skoog medium supplemented with 5, 20, or 40 g/L Suc at 20°C under a 16-h-light/8-h-dark regime for 3 weeks.
AKINβ3::GUS transgenic plants were previously described by Gissot et al. (2004)
Transformation of Agrobacterium tumefaciens strain LBA4404 was performed by electroporation using the Escherichia coli pulser transformation apparatus (Bio-Rad). Arabidopsis ecotype C0 was transformed using the floral-dip method (Clough and Bent, 1998
Total Arabidopsis RNA were isolated with TRIzol, according to the recommendations of the firm (Invitrogen). Samples were harvested in the middle of the light regime. RNA were electrophoresed, blotted, and hybridized as previously described (Bouly et al., 1999
Expression of AKINβ1 and AKINβ2 was accomplished by inserting their cDNAs into the 2µ expression vector pNSG2 (gift of Drs. N. Glab and S. Jasinsky, Institut de Biotechnologie des Plantes). These vectors were transformed into freshly prepared sip1
To prepare fusions between AKINβ1 and the Gal4 activation domain (AD) or binding domain (BD), specific AKINβ1 oligonucleotides (5'-ATGGGAAATGCGAACGGC-3' and 5'-CCGTGTGAGCGG-3') modified with 5' EcoRI and 3' BamHI restriction sites were used to amplify the full-length AKINβ1. This amplicon was then cloned in pGBKT7 and pGADT7 vectors (Clontech) to produce BD-β1/AD-β1. The same strategy was used to clone the full-length cDNAs of AKIN The BD and AD constructs were used to transform the yeast strain H7FC and protein interactions were assayed by monitoring growth on SD – Leu – Trp – His + 3 Amino-Triazol 5 mM medium (SD – LTH + 3AT 5 mM), at 30°C. The two-hybrid experiments presented in Figure 6D are representative of eight clones obtained from two independent experiments. The vectors described above were used to produce 35S-Met-labeled proteins by in vitro transcription/translation using a TNTT7 quick transcription/translation lysate system (Promega). Six milligrams of ProteinA-Sepharose (Sigma P3391) was incubated with or without 5 µL of labeled NR2 in 400 µL of buffer I (MOPS 25 mM pH 7.5, NaCl 50 mM, glycerol 10% [v/v], bovine serum albumin 6 mg/mL, EDTA 1 mM, Tween 20 0.5% [v/v], NaN3 0.02% [v/v]), at 4°C for 1 h. Five microliters of a labeled protein (or peptide) was added for one more hour. The Sepharose beads were then centrifuged (5,000g) and washed eight times with 1 mL of the buffer I. Proteins were then detached from the ProteinA-Sepharose in 20 µL of Laemmli buffer at 85°C for 5 min and separated in SDS-PAGE (10%–15% [w/v] acrylamide). The gel was dried and exposed to x-ray film overnight at room temperature. Interaction was considered positive by comparing the binding of the partner of NR2 on the ProteinA-Sepharose, in the presence or absence of NR2. Each in vitro interaction assay has been performed at least three times.
Arabidopsis Genome Initiative numbers of genes studied in this report: At3g29160 (AKIN
We thank M. Schmidt for the yeast mutants and N. Glab for the pNSG2 vector. We wish to thank Jean Vidal, A. Atteia, and F. Moreau for their critical reading of the manuscript. We are grateful to I. Gy for the sequencing, J.-P. Bares and G. Santé for growing the plants, and R. Boyer for the photographs. Received May 15, 2008; accepted August 11, 2008; published September 3, 2008.
1 This work was supported by the Ministère de l'Education Nationale et de la Recherche, France (to C.P., M.J., L.G., and P.C.). 
2 Present address: Laboratoire de Bioénergétique Fondamentale et Appliquée, INSERM U884, Université Joseph Fourier, F–38041 Grenoble, France.
3 Present address: Laboratoire de Biologie Cellulaire, Laboratoire Commun de Cytologie, INRA Versailles, RD10, Route de Saint Cyr, F–78026 Versailles cedex, France. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Martine Thomas (martine.thomas{at}u-psud.fr).
[C] Some figures in this article are displayed in color online but in black and white in the print edition.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.108.123026 * Corresponding author; e-mail martine.thomas{at}u-psud.fr.
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ABSTRACT
RESULTS
, Control lane containing NR2 alone. A star indicates the position of the AKIN subunit or subdomain tested. For each interaction tested, results are summarized at the bottom of tables (+ for a positive interaction and – for no interaction). Since AKINβ3 is constituted only by a KIS and an ASC domain, full-length (FL) and the [KIS/ASC] fragment correspond to the same sequences and thus the assay versus Nter (N terminus) does not exist. C, Control for cell-free interaction assays using luciferase, a protein which does not interact with NR2. On the right, an aliquot of luciferase in vitro translation assay (Tra) is used as a control of translation efficiency. D, Two-hybrid results are representative of eight clones obtained from two independent experiments. Clones are plated on SD – LTH + 3AT 5 mM, at 30°C. The interaction between AKINβ3 and AKINβ
