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American Society of Plant Physiologists Nodule-Specific Regulation of Phosphatidylinositol Transfer Protein Expression in Lotus japonicus
a Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824 3 To whom correspondence should be addressed. E-mail szczyglowskik{at}em.agr.ca; fax 519-457-3997
Phosphatidylinositol transfer proteins (PITPs) modulate signal transduction pathways and membrane-trafficking functions in eukaryotes. Here, we describe the characterization of a gene family from Lotus japonicus that encodes a novel class of plant PITP-like proteins (LjPLPs) and that is regulated in an unusual nodule-specific manner. Members of this gene family were identified based on their nucleotide sequence homology with a previously described cDNA, LjNOD16, which encodes the L. japonicus late nodulin Nlj16. Nlj16 or highly related amino acid sequences are shown to constitute C-terminal domains of LjPLPs and are suggested to function as specific plasma membrane targeting modules. The expression patterns of one member of this gene family (LjPLP-IV) revealed that LjNOD16 mRNA synthesis in nodules is the result of the transcriptional activity of a nodule-specific promoter located in an intron of the LjPLP-IV gene. This intron-borne bidirectional promoter also generates nodule-specific antisense transcripts derived from the N-terminal PITP domain coding region of the LjPLP-IV gene. We propose that Nlj16 protein synthesis and LjPLP-IV antisense transcript generation are components of an elaborate mechanism designed to control LjPLP synthesis and/or functioning in nodules.
Phosphatidylinositol transfer proteins (PITPs) are defined operationally by their ability to transfer phosphatidylinositol (PtdIns) or phosphatidylcholine (PtdCho) monomers between membrane bilayers in vitro (Cleves et al., 1991  ; Wirtz, 1991). Studies in a number of eukaryotic systems have demonstrated that PITPs function to regulate various aspects of lipid metabolism (reviewed in Cleves et al., 1991; B.G. Kearns et al., 1998; Li et al., 2000), but the first clue about their significance in vivo emerged from studies of Saccharomyces cerevisiae (Novick et al., 1980; Bankaitis et al., 1989, 1990; Aitken et al., 1990) showing their essential role in the formation of secretory vesicles and in protein transport from the Golgi complex. In vitro studies in mammalian systems have suggested that PITPs play important roles in promoting the activities of various inositol lipid-signaling pathways by regulating the production of certain phosphoinositides (Hay and Martin, 1993; Hay et al., 1995; Ohashi et al., 1995; Cunningham et al., 1996; Jones et al., 1998; Simon et al., 1998). These inositol-containing phospholipids have been shown to belong to a large and heterogeneous group of lipids with both structural and key regulatory roles in a wide range of important cellular signaling events (Drøbak et al., 1999).
Although PITPs generally are considered to promote signal transduction, physiological studies in Drosophila rdgB mutants have suggested a signal adaptation function for the RdgB PITP, the loss of which results in neurodegenerative disease of the fly retina (Milligan et al., 1997
Plant proteins similar to yeast PITPs also have been identified and characterized. These proteins include the Ssh1p and Ssh2p polypeptides from soybean and AtSEC14 from Arabidopsis (Jouannic et al., 1998
As part of a search for expressed sequence tags correlated with late stages of symbiotic root nodule development in the model legume plant Lotus japonicus, we previously identified and characterized a novel nodule-specific cDNA, LjNOD16, that corresponds to a highly abundant mRNA species present in nitrogen-fixing root nodules (Kapranov et al., 1997
In an attempt to generate further insights into the possible function of the Nlj16 protein in nodules, and in the context of earlier observations suggesting that Nlj16 may represent a truncated version of a much larger protein(s) (Kapranov et al., 1997 Here, we report an unanticipated relationship between Nlj16 and the predicted protein products of four members of a previously undescribed gene family that encode novel PITP-like proteins (LjPLPs). All members of this novel gene family share a two-domain structure consisting of an N-terminal PITP-like domain joined to a C-terminal domain composed of amino acid sequences identical to, or highly related to, nodulin Nlj16. The latter domain is suggested to function as a specific plasma membrane targeting module. We further demonstrate that LjNOD16 expression in nodule tissues results from an unusual transcriptional program that is controlled by a nodule-specific promoter located within an intron of the L. japonicus LjPLP gene (LjPLP-IV). A striking aspect of this transcriptional program is the ability of the same promoter sequence to drive, in reverse orientation, the synthesis of unusual nodule-specific antisense transcripts corresponding to the PITP domain coding region of LjPLP-IV. These data indicate the presence of a novel family of developmentally regulated genes encoding Sec14p-like proteins and suggest a role for Nlj16 in exerting a dominant negative effect apparently directed at inactivating the expression of specific LjPLPs in nodules.
LjNOD16 Shares a Region of Similarity with a Novel Class of PITP-like Genes We suggested previously that Nlj16 represents a domain module that is used more generally in higher plant proteins (Kapranov et al., 1997 ). Therefore, we initiated studies to determine whether the Nlj16 domain was present in other L. japonicus proteins. We initially focused on the isolation of LjNOD16-related cDNA species from L. japonicus nodules and characterized a single class of cDNAs in detail.
The longest cDNA clone of this class (pCR5h-24) consisted of 2453 bp predicted to encode a protein composed of two distinct domains (Figure 1)
. The C-terminal domain of this polypeptide shared significant similarity with the putative coiled-coil domain of Nlj16 (75 and 87% primary sequence identity and similarity, respectively). Interestingly, the N-terminal domain shared significant primary sequence homology with the major S. cerevisiae PITP Sec14p (39% identity and 59% similarity; Bankaitis et al., 1989
An unusual feature of the LjPLP-I cDNA is the presence of an in-frame TAG stop codon within the Sec14p-like domain at codon 222 (TAG222). To rule out the possibility that this TAG222 codon was the product of a cloning artifact, the genomic DNA region encompassing TAG222 was amplified from L. japonicus DNA by polymerase chain reaction (PCR), and the nucleotide sequences of four independently generated PCR products were determined. Two of these PCR products were found to be identical to the corresponding region of the LjPLP-I cDNA, containing TAG stop codons at equivalent nucleotide positions. Thus, the in-frame TAG222 codon appears to be genuine, and the LjPLP-I cDNA is unlikely to encode a functional protein product. Unexpectedly, the two other genomic PCR products were found to be highly similar to, but not identical with, the LjPLP-I cDNA. These genomic PCR products contained a CAG codon in place of the TAG222 codon present in LjPLP-I. These data suggest the presence of at least one other LjPLP gene in the L. japonicus genome, which we designated LjPLP-II (Figure 1). To characterize the LjPLP-II gene and its potential protein product, a 5.5-kb genomic DNA fragment containing the entire LjPLP-II coding region was cloned, and its DNA sequence was determined. The corresponding region was found to be 98% identical to the LjPLP-I cDNA at the nucleotide level and to contain an uninterrupted open reading frame (ORF) encoding 550 amino acids comprising both Sec14p- and Nlj16-like domains (Figure 1). Screening of a L. japonicus nodule-specific cDNA library with a DNA probe corresponding to the Sec14p-like domain of the LjPLP-I cDNA was used to identify additional members of the LjPLP gene family. Two new classes of cDNAs were isolated (LjPLP-III and LjPLP-IV; Figure 1). The longest of these cDNAs (LjPLP-III) was 2256 bp in length and encoded a protein of 625 amino acids, initiating with an ATG codon at nucleotide position +77 relative to the cDNA 5' end. The predicted structure of the deduced protein product of this ORF was found to be the same as the two-domain Sec14p-Nlj16 structure of the PLPs described above (Figure 1). The second class of cDNAs recovered in this screen was unusual. These cDNAs were found to correspond to endogenous antisense transcripts derived from yet another member of the LjPLP gene family (LjPLP-IV; Figure 1). In LjPLP-IV, the Sec14p-Nlj16 domain structure that typifies the LjPLP-I to LjPLP-III gene products is conserved. The initial indication of the presence of antisense LjPLP-IV transcripts in nodules was obtained in a search for ORFs in LjPLP-IV cDNAs. This revealed multiple short ORFs on the noncoding strand interrupted by intron sequences (see below). Conceptual translation of these ORFs revealed amino acid sequences sharing a high degree of similarity with the Sec14p domains of LjPLPs (Figure 1) as well as Sec14p-like proteins from other plant species (see Discussion). LjPLP-IV cDNAs differed both in size (0.5 to 1.5 kb) and in the positions of their 5' and 3' ends, but all of these cDNAs contained poly(A)+ sequences at their 3' ends, indicating that they were derived from mRNA transcripts (Figure 1). As described in detail below, these antisense transcripts appear to arise from unusual transcriptional events driven by a nodule-specific bidirectional promoter located within an intron of the LjPLP-IV gene.
Differential Expression of LjPLP Genes
LjPLP-IV gene expression was investigated using radiolabeled, strand-specific RNA probes complementary to derived antisense or sense transcripts. Interestingly, LjPLP-IV antisense transcripts were found to predominate in L. japonicus nodules (Figure 2B). The broad size distribution of the antisense transcripts found to hybridize was consistent with the size heterogeneity of the corresponding cDNAs (see above). Moreover, LjPLP-IV sense transcripts were found to be present in L. japonicus flowers and to constitute a family of closely migrating bands (Figure 2B). These data suggest the presence of a functional LjPLP-IV gene with diverse mRNA transcripts.
LjPLP-IV Antisense Transcripts and LjNOD16 mRNA Are Derived from the Same Gene
To test this hypothesis, two complementary approaches were used. First, a phage
A Bidirectional, Tissue-Specific Promoter Is Present within Intron 10 of LjPLP-IV The intron–exon structure of the coding region of LjPLP-IV was determined by comparing the corresponding nucleotide sequences of the genomic clone and the product of the RT-PCR amplification reaction. The LjPLP-IV gene was found to contain at least 14 exons and 13 introns (Figure 3). Intron 10 was the largest intron, defining the boundary between the N-terminal PITP-like domain and the C-terminal Nlj16 domain coding regions of LjPLP-IV. Because transcription of antisense LjPLP-IV RNAs and the LjNOD16 mRNA appeared to be initiated within intron 10, this region was postulated as a location for a bidirectional nodule-specific promoter.
This promoter region of the intron was proposed to reside within a 581-bp region of intron 10 bounded by the 5' ends of the longest antisense LjPLP-IV transcript and the LjNOD16 transcript (Figure 3). Two TATA box–like sequences were identified
The functionality of a nodule-specific promoter within LjPLP-IV intron 10 was demonstrated using transgenic plants. The putative 581-bp promoter region was fused in both orientations to a uidA reporter gene generating the forward construct (p-For) in the direction of LjNOD16 expression and a reverse construct (p-Rev) corresponding to LjPLP-IV antisense expression. Staining of hand-cut nodule sections clearly revealed that the putative LjPLP-IV intron 10 promoter directed  -glucuronidase (GUS) expression only in the central, infected zone of the nodule (Figure 5B). Other L. corniculatus tissues (roots, leaves, and flowers) did not reveal any significant cytological staining for GUS activity (data not shown). The p-Rev construct displayed strong GUS expression in vascular bundles of the nodule in addition to the infected zone (Figure 5B). A promoterless uidA construct was used as a negative control in these experiments. As expected, this control construct failed to generate GUS expression in the central infected zone of the nodules (Figure 5B). Although the level of resolution of these experiments did not allow the assignment of reporter gene activity to an infected versus uninfected cell-specific level, it established that there is a tissue-specific pattern directed by the LjPLP-IV intron 10 promoter that confers nodule-infected zone expression highly similar to that reported for the late nodulin Srglb3 promoter (Szczyglowski et al., 1994) and consistent with the localization of LjNOD16 mRNA to the infected cells of L. japonicus nodules (Kapranov et al., 1997). Therefore, we conclude that the LjPLP-IV intron 10 region contains a unique, bidirectional promoter activity involved in tissue (nodule)-specific gene expression.
Nlj16 Contains a Functional Plasma Membrane Targeting Domain
The Nlj16 domain of the LjPLP-IV protein contains two cysteine residues at the extreme C terminus that are preceded by a polybasic region (Figures 4 and 6F)
. These two motifs have been reported to cooperate in membrane targeting of prenylated proteins (Hancock et al., 1991
Structural Requirements for Nlj16 Domain–Mediated Plasma Membrane Targeting To further investigate this targeting phenomenon, we analyzed the individual roles of the Nlj16 polybasic domain and the CC motif in mGFP5–Nlj16 targeting to the plasma membrane. The Nlj16 CC motif was found to be necessary for targeting, as revealed by the observed diffuse distribution of mGFP5–Nlj16  CC within all accessible intracellular compartments; this localization resembled that of mGFP5 alone (Figure 6C). Although required for the localization of the chimeric protein to the plasma membrane, the CC motif was found to be insufficient for targeting by itself. Rather, mGFP5 localization to the plasma membrane required both the polybasic region and the CC motif (Nlj16 residues KKKQKKKTFFCC; data not shown).
As indicated above, the LjPLP-IV Nlj16 domain is very similar to the C-terminal domains of other PLP proteins from L. japonicus and other plant species (Figure 6F). Notable differences include variations in the C-terminal amino acids of these proteins; for example, the residues corresponding to the LjPLP-IV CC motif are CW and WA in LjPLP-III and LjPLP-II, respectively (Figure 6F). Further transient expression experiments demonstrated that the Nlj16-like domain of LjPLP-III (Nlj16-III) also is able to function as a plasma membrane targeting domain and that the CW motif is essential for this function (data not shown). In contrast to Nlj16, however, the C-terminal basic region of Nlj16-III (RQAEAKLRKKRFCW) was found to be insufficient to direct mGFP5 to the plasma membrane (data not shown). These results indicate that other, as yet unidentified, signals may be required for the plasma membrane targeting activity of Nlj16-III. In this regard, the likelihood that Nlj16 or Nlj16-like domains form coiled-coil structures suggests that, in addition to their potential to interact electrostatically (via charged C-terminal domains) with plasma membrane phospholipids, the Nlj16 domains also may interact with as yet unidentified protein partners (Kapranov et al., 1997
The LjPLP-IV Sec14p-like Domain Complements a Yeast sec14 Mutant Phenotype
Constitutive expression of LjPLP-IV driven by the yeast phosphoglycerate kinase (PGK) promoter failed to rescue the growth of a temperature-sensitive sec14-1 yeast strain at the restrictive temperature (Figure 7A , construct pGK-IV). However, expression of the LjPLP-IV
LjPLP-IV Exhibits Intrinsic PtdIns and PtdCho Transfer Activities in Vitro To obtain more direct evidence that LjPLP-IV is a classic PITP, we expressed a recombinant LjPLP-IV Sec14p domain (LjPLP-IV–Sec14p) in Escherichia coli and measured PtdIns and PtdCho transfer activities in crude E. coli cytosolic fractions. In control experiments, recombinant Sec14p cytosolic fractions were able to transfer 10.6% of the total input 3H-PtdIns at the highest concentration tested. Cytosolic fractions prepared from bacteria expressing LjPLP-IV–Sec14p were able to catalyze the in vitro transfer of 11.6% of input 3H-PtdIns from donor to acceptor membranes (Figure 7B).
Similar results were obtained when PtdCho transfer activities were measured (Figure 7C). Bacterial cytosolic fractions harboring recombinant Sec14p catalyzed vigorous rates of PtdCho transfer activities (10% of total input substrate transferred). Recombinant LjPLP-IV–Sec14p cytosolic fractions also exhibited significant PtdCho transfer activities (5.6% of total input 14C-PtdCho transferred at the highest cytosol concentration tested; Figure 7C). These data demonstrate that LjPLP-IV is a PITP that affects both PtdIns and PtdCho transfer. Thus, the Sec14p domain of LjPLP-IV harbors both intrinsic PtdIns and PtdCho transfer activity. These biochemical properties identify the LjPLP-IV Sec14p module as a classic PITP (Li et al., 2000
The LjPLP Family Defines a Novel Two-Domain Structure We have identified four LjPLP genes in the L. japonicus genome whose structures are characterized by a two-domain arrangement in which an N-terminal Sec14p coding region is linked to a C-terminal Nlj16 coding region. The Nlj16 and Nlj16-like C-terminal domains of LjPLPs constitute a signature of this new class of plant Sec14p-like proteins. The presence of a large C-terminal extension alone is an unusual feature for PITPs (Lopez et al., 1994 ; B.G. Kearns et al., 1998; Li et al., 2000). Yet, LjPLP structure appears to be conserved widely in higher plants. In database searches using LjNOD16, we were able to identify a number of plant genes encoding Sec14p-like proteins with C-terminal domains very similar to the putative coiled-coil domain of Nlj16. With the exception of one maize expressed sequence tag (GenBank accession number AJ006545), all of these genes are derived from the Arabidopsis genome sequencing project (e.g., GenBank accession numbers Z99708.1, AC007212.6, AL023094.2, AC006841_29, and T08565; Figure 4).
Interestingly, the two Arabidopsis expressed sequence tags (168K8 and 110G16) found previously to share similarity with the Nlj16 protein (Kapranov et al., 1997
Potential Roles for LjPLPs in Promoting Signaling
By analogy with mammalian PITPs, LjPLPs may promote phosphoinositide-driven signaling cascades initiated at the plant cell plasma membrane. Because LjPLPs appear not to be cytoplasmic proteins, their mode of action could be restricted to a PtdIns presentation mode. Because LjPLPs harbor Sec14p domains, the activities of these proteins may resemble the functions of Sec14p-like PITPs more closely than those of metazoan PITPs. In this regard, a family of nonclassic PITPs, yeast Sec14p homologs (SFH proteins), have been described that resemble LjPLPs in their membrane association properties (Li et al., 2000
Downregulation of LjPLP-IV Function in Nodules The developmentally regulated expression of antisense RNAs that derive from the LjPLP-IV Sec14p domain coding region and the expression of nodulin Nlj16 suggest that LjPLP-IV function is suppressed in nodules. Antisense RNA expression would be expected to reduce LjPLP-IV expression, and levels of LjPLP-IV sense mRNA are much lower in nodules than in flowers. Furthermore, nodulin Nlj16 expression itself could involve a developmental reprogramming of transcription within the LjPLP structural gene to direct the synthesis of a protein that represents a truncated LjPLP-IV lacking the Sec14p domain. Thus, Nlj16 might act in synergy with the antisense RNAs in blocking LjPLP-IV activity in nodules. Because nodulin Nlj16 likely is targeted to the plasma membrane, it may act as a dominant negative form of LjPLP-IV. Thus, Nlj16 might compete for a specific binding site or partner that normally interacts with LjPLP-IV or other LjPLP proteins, thereby preventing LjPLP-related biological function(s) in this plant organ.
The putative downregulation of LjPLP function in nodules may be relevant to the role of plant phospholipid metabolism in promoting the symbiosis between legumes and their endosymbionts. The activation of lipid signaling pathways in association with Nod factor–mediated root hair deformation in Vicia sativa subsp nigra has been postulated (den Hartog et al., 2001
Finally, because sense and antisense LjPLP-IV transcripts likely coexist in L. japonicus nodules, double-stranded RNA species could be generated. Such double-stranded RNA molecules, in addition to their presumed inhibitory role in LjPLP gene expression in nodules, could serve as signaling molecules involved in the long-distance coordination of plant developmental processes related to symbiotic nitrogen fixation (e.g., signaling between nodules and flowers). This signaling could occur in a manner similar to the phenomenon of post-transcriptional gene silencing (Waterhouse et al., 1998
Plant Material and Growth Conditions Lotus japonicus ecotype B-129-S9 Gifu plants were germinated and grown as described (Kapranov et al., 1997 ; Szczyglowski et al., 1997). Nodules, leaves, and stems of L. japonicus plants inoculated with Mezorhizobium loti strain NZP2235 (Jarvis et al., 1982) were harvested 35 days after inoculation; control uninoculated roots were collected from axenically grown L. japonicus plants of the same age. L. japonicus flowers were obtained from 2- to 3-month-old plants.
Transgenic L. corniculatus plants were grown as described (Szczyglowski et al., 1994
Screening of L. japonicus Genomic DNA and Nodule-Specific cDNA Libraries
Nucleic Acid Isolation and RNA Gel Blot Analyses
Radiolabeled RNA probes were prepared as follows. Template DNA (0.5 to 1 µg) was linearized and incubated in a buffer containing 40 mM Tris, pH 7.5, 8 mM MgCl2, 2 mM spermidine, 25 mM NaCl, 10 mM DTT, 40 units of placental RNase inhibitor (Boehringer Mannheim Biochemicals, Indianapolis, IN), 0.5 mM ATP, 0.5 mM GTP, 0.5 mM CTP, 15 µM UTP, 50 µCi of
Polymerase Chain Reaction Amplification and DNA Sequencing
A 5.5-kb genomic DNA fragment corresponding to the entire coding region of the LjPLP-II gene was amplified by PCR from the corresponding phage lysate by using forward (DB562) and reverse (DB561) primers. These primers were designed based on the nucleotide sequences of the 5' and 3' untranslated regions (UTRs), respectively, of LjPLP-I cDNA. PCR was performed for 30 cycles using Pfu DNA polymerase (Promega) under the following cycling conditions: a 1-min denaturation step at 94°C, a 1-min annealing step at 55°C, and a 7-min extension step at 72°C. The PCR product was cloned and sequenced. Reverse transcription (RT)–PCR was performed essentially as described (Szczyglowski et al., 1998
Chimeric Gene Constructs and Generation of Transgenic L. corniculatus Plants
The binary vectors described above were transferred independently into Agrobacterium rhizogenes A4 (Tempe and Casse-Delbart, 1989
Subcellular Localization of the mGFP5–Nlj16 Fusion Protein in Onion Epidermal Cells
Yeast Complementation Experiments
Plasmids YEplac195PGK, pGK-IV, pGK-IV
Phosphatidylinositol and Phosphatidylcholine Transfer Assays
We thank Ryan Bushey for excellent technical assistance with generation of transgenic plants and Drs. Mark Johnson and Jim Kastenmayer for their helpful advice during the course of the work. We also thank Marlene Cameron and Kurt Stepnitz for their expert help with preparation of the figures. P.K., F.J.d.B., and K.S. were supported by United States Department of Energy Grants DE-FG02-91ER20021 and 98-35305-6551 from the United States Department of Agriculture. S.M.R. and V.A.B. were supported by Grant GM44530 from the National Institutes of Health.
1 Current address: Affymetrix, 3380 Central Expressway, Santa Clara, CA 95051. 
2 Current address: Laboratoire de Biologie Moleculaire des Relations Plantes-Microorganismes, Institut National de la Recherche Agronomique/Centre National de la Recherche Scientifique, B.P. 27 31326 Castanet-Tolosan Cedex, France. Received February 14, 2001; accepted April 11, 2001.
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Abstract
INTRODUCTION
25% amino acid identity (36 to 50% similarity) with the S. cerevisiae Sec14p protein but do not have any sequence similarity with mammalian PITPs and appear to have different biochemical properties compared with the corresponding yeast and metazoan PITPs (Jouannic et al., 1998
-helical regions with a high propensity to form coiled-coil structures and a positively charged C terminus (Kapranov et al., 1997
clone containing LjNOD16 was isolated from a L. japonicus genomic DNA library. DNA sequence analysis of this clone revealed the presence of a region encoding a Sec14p-like domain, with a nucleotide sequence of the noncoding strand identical to the LjPLP-IV antisense transcripts, immediately upstream of the LjNOD16 gene (
