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First published online September 10, 2008; 10.1104/pp.108.123356 Plant Physiology 148:1497-1509 (2008) © 2008 American Society of Plant Biologists
XA27 Depends on an Amino-Terminal Signal-Anchor-Like Sequence to Localize to the Apoplast for Resistance to Xanthomonas oryzae pv oryzae1,[W]Temasek Life Sciences Laboratory, National University of Singapore, Singapore 117604, Republic of Singapore
The rice (Oryza sativa) gene Xa27 confers resistance to Xanthomonas oryzae pv oryzae, the causal agent of bacterial blight disease in rice. Sequence analysis of the deduced XA27 protein provides little or no clue to its mode of action, except that a signal-anchor-like sequence is predicted at the amino (N)-terminal region of XA27. As part of an effort to characterize the biochemical function of XA27, we decided to determine its subcellular localization. Initial studies showed that a functional XA27-green fluorescent protein fusion protein accumulated in vascular elements, the host sites where the bacterial blight pathogens multiply. The localization of XA27-green fluorescent protein to the apoplast was verified by detection of the protein on cell walls of leaf sheath and root cells after plasmolysis. Similarly, XA27-FLAG localizes to xylem vessels and cell walls of xylem parenchyma cells, revealed by immunogold electron microscopy. XA27-FLAG could be secreted from electron-dense vesicles in cytoplasm to the apoplast via exocytosis. The signal-anchor-like sequence has an N-terminal positively charged region including a triple arginine motif followed by a hydrophobic region. Deletion of the hydrophobic region or substitution of the triple arginine motif with glycine or lysine residues abolished the localization of the mutated proteins to the cell wall and impaired the plant's resistance to X. oryzae pv oryzae. These results indicate that XA27 depends on the N-terminal signal-anchor-like sequence to localize to the apoplast and that this localization is important for resistance to X. oryzae pv oryzae.
Plant disease resistance (R) genes confer race-specific resistance to pathogens that have cognate avirulence (Avr) genes (Flor, 1971  ). The R protein presumably functions as part of a receptor complex that recognizes the Avr protein and subsequently initiates defense responses (Hammond-Kosack and Jones, 1997; Martin et al., 2003). The majority of R proteins fall into five classes based primarily upon the combination of a limited number of structural motifs that they contain, while a few other R proteins have novel structures (Dangl and Jones, 2001; Martin et al., 2003). One of the interesting aspects of R protein function is their subcellular localization. Several examples of direct physical interactions between R and Avr proteins have been demonstrated (Scofield et al., 1996; Tang et al., 1996; Jia et al., 2000; Leister and Katagiri, 2000; Kim et al., 2002). Viral effectors are present inside the plant cell, and the predicted structures of all known R proteins against viruses indicate that they are also intracellular (Burch-Smith et al., 2007). The tomato (Solanum lycopersicum) Cf proteins, which recognize extracellular Cladosporium fulvum Avr proteins (Lauge and De Wit, 1998), are localized to the plasma membrane (Rivas and Thomas, 2005). Fungal pathogen-directed R proteins can also be intracellular, as fungal Avr proteins are delivered to and function inside plant cells (Jia et al., 2000). Similarly, all bacteria-directed R proteins are predicted to be intracellular, with the exception of XA21 (Song et al., 1995), because most of the bacterial Avr effector proteins are secreted into the host cells through the bacterial type III secretion system (He et al., 2004).
However, many R proteins do not carry recognizable subcellular targeting signatures, and their actual subcellular localization needs to be determined experimentally. For instance, Arabidopsis (Arabidopsis thaliana) RPM1 and RPS2 are associated with cellular membranes, although they do not possess any canonical membrane-targeting domains (Boyes et al., 1998
Bacterial blight, caused by Xanthomonas oryzae pv oryzae, is one of the most destructive bacterial diseases of rice (Mew, 1987
Functional XA27-GFP Localizes to the Apoplast
To investigate XA27 localization, we generated transgenic plants in a Nipponbare background that carried an XA27-GFP fusion gene under the control of either the native Xa27 promoter (PXa27:XA27-GFP:TXa27) or the maize (Zea mays) ubiquitin gene promoter (PUbi: XA27-GFP:TNos; Table I
). Seven resistant transgenic PXa27:XA27-GFP:TXa27 lines were generated, and line 22 (L22) was selected for further analysis. L22 carried a single copy of the PXa27:XA27-GFP:TXa27 gene and retained race-specific resistance to PXO99A (Fig. 2A
; Table II
). The PXa27:XA27-GFP:TXa27 gene in L22 expressed at a low level constitutively, which might have resulted from leaky activity of the Xa27 promoter (Fig. 2B). The PXa27:XA27-GFP:TXa27 gene in L22 was induced after inoculation with PXO99A but not with compatible X. oryzae pv oryzae strain PXO99AME1, in which avrXa27 is disrupted (Gu et al., 2005
Leaf cross sections from the immediate vicinity of the infected sites in L8 of PUbi:GFP:TNos, L9 of PUbi:XA27-GFP:TNos, and L22 of PXa27:XA27-GFP:TXa27 were subjected to confocal microscopy. The GFP fluorescence in L8 was strong, especially in mesophyll parenchyma cells (Fig. 3A ). Although the fluorescence intensity in L9 was weaker than that in L8, the XA27-GFP protein was evenly distributed among vascular bundles and mesophyll tissues (Fig. 3B). The expression of GFP in L8 or XA27-GFP in L9 did not change after bacterial inoculation with PXO99A (data not shown). A low level of XA27-GFP was detected in uninoculated L22 plants, due to leaky expression of the PXa27:XA27-GFP:TXa27 gene (Fig. 3C). XA27-GFP was strongly induced in vascular bundles of L22 plants at 3 d after inoculation (DAI) with PXO99A. It was mainly accumulated in the vascular elements, including xylem vessels, protoxylem, and phloem (Fig. 3D). However, the expression of PXa27:XA27-GFP:TXa27 in mesophyll parenchyma cells of L22 did not change significantly after bacterial inoculation (Fig. 3, C and D).
How does XA27-GFP come to be localized in xylem vessels and protoxylem, which consist of apoplast structures? One possibility is that it might be secreted from the neighboring xylem parenchyma cells. To test this possibility, we studied the localization of XA27-GFP in leaf sheath and root cells of L9 and L22. To make it easy to identify the cell wall, we induced plasmolysis in the leaf sheath or root tissues by treatment with a high-osmolarity solution. The control GFP protein in L8 was found in both the cytosol and the nucleus (Fig. 4, A and C ; Supplemental Fig. S1A). After plasmolysis, no GFP protein was detected on the cell walls of leaf sheath or root cells of L8 (Fig. 4, B and D). In contrast, fluorescent spots appeared along the borders of leaf sheath cells of L9, which could be XA27-GFP-containing vesicles (see below; Fig. 4E). After plasmolysis, XA27-GFP was detected on the cell walls of both leaf sheath and root cells (Fig. 4, F and H). Compared with leaf sheath cells, XA27-GFP was more evenly distributed on root cell walls (Fig. 4G). In addition, XA27-GFP proteins were detected in the perinuclear region, producing a fluorescent nuclear halo (Fig. 4, E and G). 4',6-Diamidino-2-phenylindole staining also indicated that XA27-GFP did not localize to the nucleus (Supplemental Fig. S1B). This perinuclear protein might be associated with the endoplasmic reticulum. Although a smaller amount of XA27-GFP was detected in L22, the localization patterns of XA27-GFP in the leaf sheath and the root cells of L22 were similar to that in L9 (Supplemental Fig. S2).
XA27-FLAG Translocates to the Apoplast via Electron-Dense Vesicles To further determine the subcellular localization of XA27, we fused XA27 with the FLAG epitope tag and performed immunogold electron microscopy to visualize XA27-FLAG in transgenic PXa27:XA27-FLAG:TXa27 plants (XA27-GFP could not be recognized by commercial anti-GFP antibodies). Forty-three independent transgenic PXa27:XA27-FLAG:TXa27 lines were generated. Line 18 (L18F) was selected for further analysis because it carried a single copy of the PXa27:XA27-FLAG:TXa27 gene. This line conferred complete resistance to PXO99A and displayed moderate susceptibility to PXO99AME1 (Fig. 2A; Table II). The PXa27:XA27-FLAG:TXa27 gene in L18F was expressed constitutively at a low level but was inducible upon inoculation with PXO99A (Fig. 2D). The XA27-FLAG protein in L18F was detected as a band with a molecular size of about 13 kD in immunoblot analysis with anti-FLAG monoclonal antibody (Fig. 2E). Leaf cross sections of L18F plants were subjected to immunogold electron microscopy. As depicted by the gold particles, XA27-FLAG was detected in the cytoplasm and the apoplast of the xylem parenchyma cells (Fig. 5, E–L ). In uninoculated L18F plants, XA27-FLAG localized mainly to electron-dense vesicles in the cytoplasm and to the cell walls of xylem parenchyma cells (Fig. 5, E and F). After inoculation with PXO99A, XA27-FLAG protein was induced to higher levels in the xylem parenchyma cells of L18F plants. Electron-dense vesicles containing XA27-FLAG were abundant at the pits between xylem parenchyma cells (Fig. 5, G–I), between xylem vessels and parenchyma cells (Fig. 5, J–K), and between xylem parenchyma cells and mesophyll parenchyma cells (data not shown). The XA27-FLAG protein was also found in the xylem vessels of inoculated L18F plants, where it localized to lumina of the xylem vessels rather than being associated with bacteria or vessel walls (Fig. 5L). XA27-FLAG appears to be secreted from electron-dense vesicles in the cytoplasm to the apoplast, perhaps via exocytosis (Fig. 5H). No XA27-FLAG protein was found to localize to the nucleus or other organelles of xylem parenchyma cells in either uninoculated or inoculated L18F plants (data not shown). In control experiments, in which preimmune serum was used to replace anti-FLAG antibody, we did not observe concentrated labeling of vesicular structures in specimens of L18F (Fig. 5, A and B). Similar results were obtained with samples of Nipponbare lacking the transgene when anti-FLAG antibody was used (Fig. 5, C and D).
The N-Terminal Signal-Anchor-Like Sequence Is Required for XA27 Localization To determine whether the signal-anchor-like sequence is sufficient to explain the observed localization of XA27 to the apoplast and cell wall, we fused this sequence to GFP (N57-GFP) and generated 56 transgenic plants with the PUbi:N57-GFP:TNos gene (Table I). Line 12 (L12) of PUbi:N57-GFP:TNos was selected to study N57-GFP localization (Table II). The expression of the PUbi:N57-GFP:TNos gene in L12 was comparable to that of the PUbi:GFP:TNos gene in L8 (Supplemental Fig. S3). Like XA27-GFP, N57-GFP localized to the cell walls of leaf sheath and root cells (Fig. 6, A to D ).
To determine whether the h-region of the signal-anchor-like sequence is required for this localization, we deleted the h-region from the signal-anchor-like sequence and fused the remaining 37-amino acid n-region with GFP (N37-GFP). We generated 66 transgenic plants with the PUbi:N37-GFP:TNos gene (Table I). Line 2 (L2) of PUbi:N37-GFP:TNos was selected to study N37-GFP localization (Table II; Supplemental Fig. S3). After plasmolysis, no N37-GFP was detected on the cell walls of leaf sheath or of root cells (Fig. 6, E and F).
The triple Arg motif in the signal-anchor-like sequence of XA27 is conserved between XA27 and its paralogs in rice (Gu et al., 2005
Localization of XA27 to the Apoplast Is Required for Disease Resistance The failure of localization of XA27G-GFP to the apoplast in L18G of PUbi:XA27G-GFP:TNos and in L46 of PXa27:XA27G-GFP:TXa27 allowed us to ask whether the proper localization of the fusion protein is required for its function in conferring disease resistance. Plants expressing the XA27G-GFP proteins were not resistant to bacterial blight pathogens (Fig. 2A; Table II). These results suggest that the localization of XA27 to the apoplast is required for XA27-mediated disease resistance to X. oryzae pv oryzae. To further test this, we replaced the triple Arg motif in XA27 with Gly residues and generated transgenic plants with the PXa27:XA27G:TXa27 gene (Table I). Sixty-one independent transgenic lines were obtained, and they all carried the PXa27:XA27G:TXa27 gene (data not shown). Although the expression of PXa27:XA27G:TXa27 in these transgenic plants was comparable to that of the wild-type Xa27 transgene in transgenic line TN8 after inoculation with PXO99A (Fig. 8B ), none of the XA27G transgenic plants conferred resistance to the incompatible strain (Fig. 8A).
Xa27 is specifically induced by AvrXa27 from incompatible pathogens (Gu et al., 2005 ). In vivo in IRBB27, the expression of Xa27 is normally tightly controlled and is not induced by any other biotic and abiotic stresses (Gu et al., 2005). Nonetheless, we found that constructs containing the Xa27 promoter showed constitutive low-level expression in transgenic plants. This was true whether the transgenic plants contained genomic clones of Xa27 under the control of its native promoter (L. Wu and Z. Yin, unpublished data) or fusion genes under the control of the Xa27 promoter. We speculate that the Xa27 promoter is sensitive to its position on the rice chromosome and that the constitutive expression might be due to a position effect on the transgenes in rice chromosomes. Leaky expression of XA27 or its functional derivatives was found to provide enhanced resistance to compatible pathogen strains. This resistance was dosage dependent. In this study, we selected transgenic lines that retained resistance specificity to incompatible pathogens. The transgenes in these lines were inducible by AvrXa27. We believe that these lines are suitable for determining the localization of XA27 or its fusion proteins, because these fusion proteins confer resistance to the pathogen, indicating their functionality. In addition, the localization of XA27-GFP to the cell walls of leaf sheath and root cells in L22 of PXa27:XA27-GFP:TXa27 and in L9 of PUbi:XA27-GFP:TNos gave similar results, which indicates that subcellular localization of XA27-GFP is determined by the nature of the protein. In this case, the localization cannot be explained by any tissue specificity in transgene expression due to the promoter.
The apoplast is the extraprotoplastic matrix of plant cells, consisting of all compartments from the external face of the plasmalemma to the cell wall (Dietz, 1997 Although the biochemical function of XA27 remains to be determined, its localization to xylem vessels may contribute to local resistance to the pathogen at the infection site. XA27 appears to be secreted to the lumina of xylem vessels through the pits between xylem vessels and xylem parenchyma cells. Since xylem parenchyma cells were not suitable for plasmolysis and analysis by confocal microscopy, the localization of XA27-GFP and its derivatives to the apoplast was examined in the leaf sheath cells and in roots of transgenic plants. As the extracellular space or apoplast of leaf sheath cells and root cells is limited, compared with that of xylem vessels, the secreted XA27-GFP protein mainly localizes to the cell wall in these cases. This suggests an extracellular or apoplastic localization of XA27.
Although we lack the means to detect the location of the endogenous XA27 protein, our studies indicate that XA27-FLAG and XA27-GFP proteins localized to the apoplast. XA27 might be secreted to the apoplast by exocytosis, as XA27-FLAG was detected in both cytoplasmic electron-dense vesicles and in the apoplast. The signal-anchor-like sequence of XA27 contains a triple Arg motif, which appears to be essential for both its localization and function. Mutation of this sequence abolished XA27 localization and impaired its ability to confer disease resistance. Similar Arg motifs are also found in the signal peptides of proteins translocated through the twin Arg translocation (Tat) pathway (Robinson and Bolhuis, 2004 In conclusion, we have found that the inducible R protein XA27 localizes to the apoplast. This localization depends on a signal-anchor-like sequence at the N-terminal region of XA27 and is required for XA27-mediated resistance to X. oryzae pv oryzae. The identification of XA27 localization to the apoplast and its localization signal will facilitate further characterization of the biochemical function of the R protein.
Constructs
The constructs used in this study (Table I) were made based on binary vectors pC1300 or pC1305.1 and verified by DNA sequencing. The XA27-GFP fusion gene was generated by PCR with the Xa27 coding region amplified from NA5.2 (Gu et al., 2005
Rice (Oryza sativa) IRBB27 is a near-isogenic line of Xa27 in the IR24 background (Gu et al., 2004
Agrobacterium tumefaciens-mediated transformation of Nipponbare rice was carried out as described previously (Yin and Wang, 2000
The X. oryzae pv oryzae strains were cultured on PSA medium (10 g L–1 peptone, 10 g L–1 Suc, 1 g L–1 Glu, and 16 g L–1 bacto-agar, pH 7.0) for 2 to 3 d at 28°C. Bacteria were collected and suspended in sterile water at an optical density of 0.5 at 600 nm. Bacterial blight inoculation was carried out using the leaf-clipping method (Kauffman et al., 1973
GFP fluorescence in transgenic plants was examined on the cells of leaves, leaf sheaths, and roots. Leaves of inoculated or uninoculated plants were manually and transversely sectioned with a surgical blade (no. 10). Leaf sheath sections of about 3 x 3 mm2 and root tips of about 1 cm long were cut from 10-d-old plants. Samples were mounted in water for examination and photography. Plasmolysis was induced on leaf sheath or root cells by incubating the samples in 10% (w/v) mannitol solution for 1 h and mounting in the same solution for examination. Samples were examined for GFP fluorescence with a confocal microscope (Zeiss LSM 510 META) using the excitation/emission combination of 488/505 to 530 nm band pass. The bright-field image was taken simultaneously using Phase Contrast 2 optics.
Total RNA was isolated from rice leaves using the RNeasy Plant Mini Kit (Qiagen) according to the manufacturer's instructions. About 20 µg of total RNA was loaded in each lane for RNA gel-blot analysis. The RNA loading was assessed by staining RNA blots with methylene blue or hybridizing RNA blots with the rice Ubiquitin2 gene (Ubi). DNA probes were labeled with [32P]dCTP using the Rediprime II random prime labeling system (Amersham Biosciences).
About 20 µg of total proteins from transgenic plants was separated on 12% SDS polyacrylamide gels followed by blotting onto nitrocellulose membranes. XA27-FLAG proteins were detected with an anti-FLAG-M2 monoclonal antibody (Sigma) and horseradish peroxidase-coupled secondary antibody (Bio-Rad).
Immunogold electron microscopy was carried out according to the procedure described previously (Chye et al., 1999 Sequence data from this article can be found in the GenBank/EMBL data libraries under accession number AAY54164.
The following materials are available in the online version of this article.
We thank Xuezhi Ouyang, Ao Yin, Qingwen Lin, Dongjiang Wang, and Tze Yee Teo for technical assistance, the Center for the Application of Molecular Biology to International Agriculture for binary vectors pC1300 and pC1305.1, and Stephen Cohen and Mithilesh Mishra for critical reading of the manuscript. Received May 22, 2008; accepted September 4, 2008; published September 10, 2008.
1 This work was supported by intramural research funds from the Temasek Life Sciences Laboratory (to Z.Y.) and by a grant from the Agri-Food and Veterinary Authority of Singapore (to Z.Y.). 
2 Present address: Molecular Genetics, Agriculture and Agri-Food Canada, 107 Science Place, Saskatoon, Saskatchewan, Canada S7N 0X2. 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: Zhongchao Yin (yinzc{at}tll.org.sg).
[W] The online version of this article contains Web-only data. www.plantphysiol.org/cgi/doi/10.1104/pp.108.123356 * Corresponding author; e-mail yinzc{at}tll.org.sg.
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