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First published online July 7, 2006; 10.1104/pp.106.081109 Plant Physiology 142:45-53 (2006) © 2006 American Society of Plant Biologists Disruption and Overexpression of Arabidopsis Phytosulfokine Receptor Gene Affects Cellular Longevity and Potential for Growth1Graduate School of Bio-Agricultural Sciences, Nagoya University, Chikusa, Nagoya 464–8601, Japan
Phytosulfokine (PSK), a 5-amino acid sulfated peptide that has been identified in conditioned medium of plant cell cultures, promotes cellular growth in vitro via binding to the membrane-localized PSK receptor. Here, we report that loss-of-function and gain-of-function mutations of the Arabidopsis (Arabidopsis thaliana) PSK receptor gene (AtPSKR1) alter cellular longevity and potential for growth without interfering with basic morphogenesis of plants. Although mutant pskr1-1 plants exhibit morphologically normal growth until 3 weeks after germination, individual pskr1-1 cells gradually lose their potential to form calluses as tissues mature. Shortly after a pskr1-1 callus forms, it loses potential for growth, resulting in formation of a smaller callus than the wild type. Leaves of pskr1-1 plants exhibit premature senescence after bolting. Leaves of AtPSKR1ox plants exhibit greater longevity and significantly greater potential for callus formation than leaves of wild-type plants, irrespective of their age. Calluses derived from AtPSKR1ox plants maintain their potential for growth longer than wild-type calluses. Combined with our finding that PSK precursor genes are more strongly expressed in mature plant parts than in immature plant parts, the available evidence indicates that PSK signaling affects cellular longevity and potential for growth and thereby exerts a pleiotropic effect on cultured tissue in response to environmental hormonal conditions.
Plants, due to their sessile nature, have developed a greater ability to adapt to dynamic environmental conditions than have animals. This plasticity allows plants to flexibly alter their developmental program and metabolism according to the environment. A particularly important adaptation of this type is the ability to form calluses from almost any plant tissue. However, studies suggest that a population of living cells is often required to support callus growth in vitro even if sufficient amounts of growth regulators and nutrients are supplied. This population dependence is alleviated by addition of conditioned medium in which cells have previously been grown, indicating that such cell-to-cell communication is mediated by chemical signal(s) produced by growing cells (Bellincampi and Morpurgo, 1987  ; Birnberg et al., 1988).
Phytosulfokine (PSK), a 5-amino acid sulfated peptide that has been detected in conditioned medium of plant cell cultures, is the primary signal molecule responsible for this cell-to-cell communication (Matsubayashi and Sakagami, 1996
PSK is produced from approximately 80-amino acid precursor peptides via posttranslational sulfation of Tyr residues and proteolytic processing (Yang et al., 1999
PSK binds the membrane-localized PSK receptor PSKR1, which is a Leu-rich repeat receptor kinase (LRR-RK) that has been purified from solubilized carrot (Daucus carota) microsomes by ligand-based affinity chromatography (hereafter referred to as DcPSKR1; Matsubayashi et al., 2002
Studies revealing the in vitro function of PSK and the molecular basis of ligand-receptor interaction in PSK signaling have paved the way for research aimed at characterization of the in vivo role of PSK and its downstream signaling pathway in plants. The carrot PSK receptor, DcPSKR1, exhibits high-percentage amino acid identity with one LRR-RK found in the Arabidopsis (Arabidopsis thaliana) genome. Also, a database search has revealed the presence of five paralogous PSK precursor genes in the Arabidopsis genome. In this study, we analyzed the Arabidopsis PSK receptor gene using gain-of-function and loss-of-function strategies and found that PSK signaling in plants affects their potential for growth and cellular longevity. We also examined the expression patterns of all five paralogous PSK precursor genes in the Arabidopsis genome using promoter-
Five Paralogous PSK Precursor Genes in Arabidopsis
Upon analyzing the in planta role of PSK signaling, we first identified all the PSK precursor genes in Arabidopsis. In addition to two PSK precursor genes (At2g22860 and At3g49780) previously identified and confirmed to encode the functional PSK (Yang et al., 2001
Expression Patterns of PSK Precursor Genes in Arabidopsis Northern blotting revealed that AtPSKs are expressed in a variety of tissues including roots, leaves, stems, flowers, siliques, and calluses, with the exception of AtPSK1, which was only expressed in roots (Fig. 1C). AtPSK2, AtPSK4, and AtPSK5 were more strongly expressed in lower mature leaves than in upper young leaves (Fig. 1D), suggesting that the main in planta role of PSK is in plant homeostasis rather than morphogenesis. In addition, expression of AtPSK4 is highly up-regulated upon mechanical wounding (Fig. 1E). To further analyze expression patterns of AtPSKs, we generated transgenic Arabidopsis plants harboring AtPSK promoter-GUS reporter gene constructs. Among the above-ground plant parts assayed, the constructs pAtPSK2::GUS, pAtPSK3::GUS, pAtPSK4::GUS, and pAtPSK5::GUS were widely expressed in cotyledons and leaves and were most abundantly expressed in vascular bundles (Fig. 1F). In roots, pAtPSK3::GUS was primarily expressed in root tips, whereas expression of pAtPSK2::GUS, pAtPSK4::GUS, and pAtPSK5::GUS was mainly detected in the more mature regions of the root. Within 12 h after leaf discs were cut, expression of AtPSK4 had greatly increased at their outer edges, indicating that the AtPSK4 promoter is activated by wounding (Fig. 1G).
We generated transgenic Arabidopsis plants that overexpressed AtPSK4, the most prominently expressed PSK precursor gene throughout the Arabidopsis tissues, under the control of the 35S promoter, and named these plants AtPSK4ox. AtPSK4ox plants germinated normally and developed normal cotyledons and hypocotyls phenotypically indistinguishable from wild type. Growth of AtPSK4ox seedlings, especially root growth, was somewhat faster than wild-type growth (Fig. 1H). However, the overall growth of above-ground parts of AtPSK4ox plants was indistinguishable from that of wild type (data not shown). Growth of AtPSK4ox calluses derived from the leaves of 3-week-old plants was somewhat faster than growth of wild-type calluses (Fig. 1I).
To analyze PSK signaling in Arabidopsis, we searched for the Arabidopsis PSK receptor, based on overall amino acid similarity to DcPSKR1, and determined that At2g02220 is most likely an ortholog of DcPSKR1. At2g02220 encodes a 1,008-amino acid LRR-RK that has 60% amino acid sequence identity to DcPSKR1 and contains 21 tandem copies of LRR, a 36-amino acid island domain between the 17th and 18th LRR, a single transmembrane domain, and a cytoplasmic kinase domain (Fig. 2A
). Amino acid sequences in the island domain are highly conserved between DcPSKR1 and At2g02220 (Fig. 2B). An island domain has also been found among the extracellular LRRs of the brassinosteroid receptor BRI1 and has been shown to be involved in ligand binding (Kinoshita et al., 2005
To determine whether At2g02220 protein specifically interacts with PSK, we first overexpressed At2g02220 in Arabidopsis plants under the control of a constitutive 35S promoter and established suspension cell lines derived from these transgenic plants by inducing callus formation from leaf discs (overexpressor [OX1] cell line). We observed some increase in [3H]PSK binding activity in the membrane fractions of the transgenic calluses, but neither the transgenic plants nor the transgenic calluses exhibited specific phenotypes (data not shown). In western blotting of microsomal fractions from cells using an anti-At2g02220 antibody, two distinct bands were recognized by the antibody: a 120-kD protein and a 150-kD protein. Compared to wild-type cells, the expression level of the 120-kD protein was increased in the transgenic cells, but the expression level of the 150-kD protein was unchanged, possibly due to posttranslational regulation (Fig. 2D).
We next overexpressed At2g02220 in Arabidopsis plants by increasing its copy number and established suspension cell lines derived from these plants by inducing callus formation from leaf discs (OX2 cell line). We observed a significant increase in [3H]PSK binding activity in the membrane fractions of the OX2 transgenic cells (Fig. 2E). Scatchard analysis of the binding data indicated that [3H]PSK binds At2g02220 with a dissociation constant (Kd) of 7.7 ± 0.9 nM, which is similar to the Kd of DcPSKR1 (Matsubayashi et al., 2002
To examine the physiological function of AtPSKR1, we performed a database search for loss-of-function AtPSKR1 mutants and found a Ds insertion mutant (hereafter referred to as pskr1-1) at the AtPSKR1 locus in transposon-tagging lines released by the Institute of Molecular Agrobiology, the National University of Singapore (Fig. 3A
; Parinov et al., 1999
Phenotypes of Loss-of-Function and Gain-of-Function Mutants of AtPSKR1 We compared the phenotypes of the AtPSKR1 knockout (pskr1-1) and the AtPSKR1 OX2 line (hereafter referred to as AtPSKR1ox) with the wild-type phenotype. AtPSKR1ox and pskr1-1 seedlings grown on B5 agar plate germinated normally and developed normal cotyledons and hypocotyls phenotypically indistinguishable from wild type. Root growth of pskr1-1 seedlings was slightly reduced, whereas root growth of AtPSKR1ox was comparable to that of wild type (Fig. 3E). In the first 3 weeks of culture on B5 agar, there were no morphological differences in overall growth of above-ground plant parts between pskr1-1, AtPSKR1ox, and wild type (Fig. 3F, leftmost section). The most striking phenotype of the pskr1-1 plants was that individual cells gradually lost their potential to form calluses as the tissues matured (Fig. 3F, bottom). Leaf discs from the fully expanded leaves of pskr1-1 plants exhibited severe defects in hormone-induced callus formation. Young immature pskr1-1 leaves close to the meristem retained full callus-forming potential. Leaf discs of wild-type plants exhibited high potential for callus formation irrespective of the age of the leaves. Complementation of homozygous pskr1-1 plants with a wild-type 6.5-kb EcoRV/BlnI genomic fragment of AtPSKR1 restored their callus-forming potential, confirming that the phenotypes of homozygous pskr1-1 plants were caused by the disruption of AtPSKR1 (Fig. 3G, top). The pskr1-1 mutant can also be functionally complemented by expressing the cDNA of the carrot DcPSKR1 gene under the control of the Arabidopsis AtPSKR1 promoter, suggesting that AtPSKR1 and DcPSKR1 function in the same pathway (Fig. 3G, bottom). In contrast, leaf discs of AtPSKR1ox plants exhibited a significantly greater callus-forming potential than wild type, irrespective of the age of the leaves (Fig. 3F, top).
There were also significant differences in relative growth rate of calluses between pskr1-1, AtPSKR1ox, and wild type. The pskr1-1 calluses exhibited premature senescence with browning within 3 weeks of culture, resulting in formation of a smaller callus than the wild type after 6 weeks (Fig. 3H, left). The senescence marker SEN1 transcript (Oh et al., 1996 The pskr1-1 seedlings grew at almost the same rate as wild-type seedlings, flowered normally, and completed the normal life cycle, but their leaves exhibited premature senescence phenotypes 4 weeks after germination (Fig. 4A ). All the leaves of pskr1-1 plants were senesced 6 weeks after germination (Fig. 4, B and D). The AtPSKR1ox seedlings also grew at almost the same rate as wild-type seedlings and completed the normal life cycle, but they developed larger leaves than the wild type (Fig. 4C) and exhibited delayed senescence (Fig. 4, B and D). This enlargement of leaves was due to an increase in cell number but not an increase in cell size (data not shown).
Expression patterns of AtPSKs are consistent with the greater severity of pskr1-1 phenotypes in the lower mature leaves where AtPSKs are more strongly expressed. All these results strongly suggest that PSK signaling in plants affects their potential for growth and cellular longevity.
Our findings indicate that the At2g02220 gene encodes a functional PSK receptor (AtPSKR1) in Arabidopsis. AtPSKR1 is a member of the LRR-RK family and is characterized by 21 tandem copies of extracellular LRR, a 36-amino acid island domain between the 17th and 18th LRR, a single transmembrane domain, and a cytoplasmic kinase domain. AtPSKR1 interacts with [3H]PSK with a Kd of 7.7 ± 0.9 nM, which is similar to the Kd of DcPSKR1 (4.2 ± 0.4 nM).
PSK receptors are often detected on SDS-PAGE as two distinct bands with different molecular size (Matsubayashi and Sakagami, 2000
In this study, although seedlings of pskr1-1 exhibited normal growth and developed rosette leaves phenotypically indistinguishable from wild type for the first 3 weeks after germination, individual pskr1-1 cells gradually lost their potential to form calluses as tissues matured. The pskr1-1 calluses derived from immature tissues also exhibited premature senescence accompanied by browning within 3 weeks of culture, resulting in formation of a smaller callus than the wild type. Premature senescence phenotypes were also observed in leaves of pskr1-1 plants at the late bolting stage. In contrast, AtPSKR1ox calluses vigorously proliferated and did not exhibit symptoms of senescence even after 6 weeks of culture, resulting in formation of calluses almost twice the size of wild type. AtPSKR1ox plants exhibited delayed senescence, and its leaves underwent prolonged expanding growth, resulting in formation of bigger leaves than the wild type. This enlarged leaf phenotype was not obvious until the bolting stage, suggesting that it is due to continuous proliferation rather than accelerated cell division. These results strongly suggest that PSK represents a new class of hormones that affect the potential for cellular growth and longevity of individual cells but are not simple mitogens or differentiation factors. Overactivation or disruption of PSK signaling did not interfere with meristem organization or subsequent plant morphogenesis, except for the changes in cellular longevity and slight differences in root and leaf growth, which is consistent with our previous observation that treatment of dispersed mesophyll cells with PSK peptide alone does not directly induce any morphological changes (Matsubayashi et al., 1999a Our biochemical experiments confirm that Arabidopsis has five paralogous genes encoding PSK precursors (AtPSKs) that are functionally secreted after posttranslational sulfation and processing. Multiple alignment of the deduced amino acid sequences revealed that, in addition to the 5-amino acid PSK domain, certain residues between amino acid positions –25 and –1 are highly conserved among the PSK precursor peptides, including multiple acidic residues, one Cys pair, several hydrophobic residues, consecutive basic residues, and one His residue. We speculate that some of these residues synergistically determine Tyr sulfation efficiency and others are involved in proteolytic processing. Expression of AtPSKs was detected in almost all plant tissues, including fully developed mature leaves. In addition, AtPSK2, AtPSK4, and AtPSK5 were more strongly expressed in the lower mature leaves than in upper young leaves. These expression patterns are consistent with our conclusion that PSK regulates potential for cellular growth and longevity of individual cells rather than directly inducing cell division or differentiation. One of the PSK precursor genes is also highly up-regulated upon wounding, suggesting that PSK is involved in wound response signaling.
In contrast to the relatively obvious phenotypes of AtPSKR1ox plants, the only phenotypic alterations that we observed in Arabidopsis plants overexpressing PSK precursor gene were a slight increase in root growth at the seedling stage and a slight increase in callus proliferation in vitro. One possibility is that basal expression of endogenous AtPSKs is at a sufficiently high level to activate PSK signaling, and exogenous transgene-encoded PSK therefore does not cause any additional effects. Indeed, PSK shows a dose-response curve that reaches a plateau at PSK levels of around 10 nM (Matsubayashi and Sakagami, 1996
How might PSK activate the potential for cellular growth and longevity of individual cells? One may speculate that PSK modulates sensitivity to endogenous plant hormones such as auxin and cytokinin, thereby indirectly causing growth alteration. However, that hypothesis is not consistent with our finding that pskr1-1 hypocotyls can respond to auxin/cytokinin and form calluses at normal auxin/cytokinin concentrations. Moreover, in the root elongation assay, pskr1-1 seedlings exhibited the same cytokinin response as wild-type seedlings (data not shown). In animals, there is much evidence indicating that cellular growth and longevity are tightly coupled to protein translation and protein turnover via TOR (target of rapamycin) protein kinase, which is an integrator molecule of nutrient availability, growth factors, and the energy status of the cells (Martin and Hall, 2005 In contrast to the relatively clear understanding of the mechanism of maintenance of cellular homeostasis in the shoot apical meristem of plants, little is known about the molecular basis for the cellular plasticity that allows plants to flexibly alter their developmental program according to the environment. We are currently researching the downstream target of PSK signaling, using AtPSKR1ox and pskr1-1 plants.
Plant Material and Growth Conditions The Arabidopsis (Arabidopsis thaliana, Landsberg erecta [Ler]) plants were grown at 22°C under continuous light, on rockwool or on B5 medium containing 1.0% Suc solidified with 0.7% agar. For callus induction, leaf discs or hypocotyl segments were excised from donor plants grown on B5 agar plate and were cultured on callus induction medium (CIM) containing B5 medium with 0.5 mg/L 2,4-dichlorophenoxyacetic acid, 0.1 mg/L kinetin, 20 g/L Glc, 0.5 g/L MES, and 2.5 g/L gellan gum, at 22°C under continuous light. Arabidopsis (Columbia) T87 cells were maintained in B5 medium containing 1.0 µM naphthylacetic acid and 1.5% Suc by gentle agitation at 120 rpm under continuous light at 22°C.
The loss-of-function mutant of AtPSKR1 (SGT5281) was found in the searchable database of Ds insertion sequences (Ler background) released by the Institute of Molecular Agrobiology, the National University of Singapore (Parinov et al., 1999
cDNA clones coding for AtPSKs were obtained by RT-PCR from total RNA of Arabidopsis plants. Site-directed mutagenesis of AtPSK1, AtPSK3, and AtPSK5 cDNA was performed by PCR using the overlap extension technique. The resulting cDNAs were ligated into the binary vector pBI121 by replacing the GUS coding sequence downstream of the cauliflower mosaic virus (CaMV) 35S promoter. Arabidopsis T87 suspension cells were coincubated with Agrobacterium tumefaciens (C58C1) harboring these constructs for 2 d and further incubated on CIM plate containing 50 mg/L kanamycin and 200 mg/L carbenicillin for 4 weeks. The selected calluses were then transferred to suspension culture.
The AtPSKR1 (At2g02220) full-length cDNA was obtained from the RIKEN BioResource Center (Tsukuba, Japan; Seki et al., 1998
To study expression patterns of AtPSKR1, AtPSK2, AtPSK3, AtPSK4, and AtPSK5 in detail, we amplified the upstream 2.0-kb promoter regions of AtPSKR1 or the other AtPSKs by genomic PCR and cloned them by translational fusion in frame with the GUS coding sequence in the binary vector pBI101. Histochemical analysis of GUS gene expression in the transformed plants was performed as described elsewhere (Kosugi et al., 1990
Culture medium (20 mL) derived from suspensions of transgenic T-87 cells expressing mutated AtPSKs were loaded onto a DEAE Sephadex A-25 column (5.0 x 30 mm, packed in an Econo-column [Bio-Rad]) equilibrated with 20 mM Tris-HCl, pH 7.5. The column was washed with 3.0 mL of the same buffer containing 500 mM KCl, and PSKs were eluted with 1.0 mL of the same buffer containing 2,000 mM KCl. Eluate from the DEAE Sephadex A-25 column was acidified by adding formic acid at a final concentration of 1.0%. LC/MS analysis was performed using a JASCO semimicro HPLC pump system (model PU-2085) equipped with a column switching-valve unit (model HV-2080-01). Sample (200 µL) was loaded to the first reverse-phase column (Develosil ODS-HG-5 column, 2.0 x 50 mm) using 5% acetonitrile (containing 0.1% formic acid) with a flow rate of 200 µL/min. After this cleanup and enrichment step (5.0 min), the first column was connected to the second reverse-phase analytical column (Develosil ODS-HG-5 column, 2.0 x 150 mm) in back-flush mode by means of the time-controlled switching valve, and eluted with a gradient of 5%/20%/20% acetonitrile (containing 0.1% formic acid) in 0/15/20 min at a flow rate of 200 µL/min. The HPLC eluate was introduced into an electrospray ionization ion-trap mass spectrometer (LCQ Deca XP-plus, Thermo Electron) via an electrospray ionization interface at a spray voltage of 5.0 kV. The mass spectrometer was operated in negative ion mode with a capillary temperature of 220°C, a capillary voltage of –38 V, and the tube lens offset at 30 V. The mass spectra were obtained by scanning the mass range from mass-to-charge ratio 700 to 900.
An N-terminal 100-amino acid region of AtPSKR1 (excluding the signal peptide) was expressed in Escherichia coli using the pET-24b expression vector and purified as a His6 fusion. This recombinant protein was used as the antigen to generate the antibodies in rabbits and was used for affinity purification of the antibodies using Hi-Trap NHS activated Sepharose.
Tritium-labeled PSK was prepared by tritium reduction of a PSK analog containing tetradehydro-Ile (Matsubayashi and Sakagami, 1999 Sequence data from this article can be found in the GenBank/EMBL data libraries under accession numbers NM_126282 (AtPSKR1), NM_101229 (AtPSK1), NM_127851 (AtPSK2), NM_114342 (AtPSK3), NM_114838 (AtPSK4), and NM_125984 (AtPSK5).
We thank the Institute of Molecular Agrobiology, the National University of Singapore, for providing the seeds of the Ds mutant line, and RIKEN BioResource Center for providing the AtPSKR1 full-length cDNA. Received March 29, 2006; accepted July 4, 2006; published July 7, 2006.
1 This work was supported by the 21st Century Center of Excellence Program (grant no. 14COEA02), by a Grant-in-Aid for Scientific Research for Priority Areas (grant no. 14036214), and by a Grant-in-Aid for Young Scientists (A) (grant no. 18687003).  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: Yoshikatsu Matsubayashi (matsu{at}agr.nagoya-u.ac.jp). www.plantphysiol.org/cgi/doi/10.1104/pp.106.081109 * Corresponding author; e-mail matsu{at}agr.nagoya-u.ac.jp; fax 81–52–789–4118.
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-glucuronidase (GUS) analysis. In this article, we discuss possible functions of PSK signaling. 
contributes to the pollen population effect. Planta 211: 752–755
