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J Exp Bot. Feb 2009; 60(2): 641–650.
Published online Dec 16, 2008. doi:  10.1093/jxb/ern316
PMCID: PMC2651452
Darwin Review

Molecular responses of Lotus japonicus to parasitism by the compatible species Orobanche aegyptiaca and the incompatible species Striga hermonthica

Abstract

Lotus japonicus genes responsive to parasitism by the compatible species Orobanche aegyptiaca and the incompatible species Striga hermonthica were isolated by using the suppression subtractive hybridization (SSH) strategy. O. aegyptiaca and S. hermonthica parasitism specifically induced the expression of genes involved in jasmonic acid (JA) biosynthesis and phytoalexin biosynthesis, respectively. Nodulation-related genes were almost exclusively found among the Orobanche-induced genes. Temporal gene expression analyses revealed that 19 out of the 48 Orobanche-induced genes and 5 out of the 48 Striga-induced genes were up-regulated at 1 dai. Four genes, including putative trypsin protease inhibitor genes, exhibited systemic up-regulation in the host plant parasitized by O. aegyptiaca. On the other hand, S. hermonthica attachment did not induce systemic gene expression.

Keywords: Host response, Lotus japonicus, Orobanche, Striga, suppression subtractive hybridization

Introduction

Orobanche and Striga spp. are obligate root parasitic plants that affect the production of several agronomically important crops in many parts of the world. Among Orobanche spp., O. aegyptiaca and O. ramosa have the widest host range, including plants belonging to the following families: Solanaceae, Fabaceae, Brassicaceae, Cucurbitaceae, Asteraceae, Umbelliferae, Cannabinaceae, and Linaceae (Goldwasser and Kleifeld 2004). Striga spp. exhibit great diversity in the semi-arid grasslands of Africa where three wide-ranging species, namely, S. asiatica, S. gesnerioides, and S. hermonthica are serious agronomic pests (Musselman et al., 1983). Of these three species, S. hermonthica mainly parasitizes tropical cereal crops and is the most devastating root parasite in Africa (Berner et al., 1995). The ultimate method for control of parasitic plants lies in the development of crops that are resistant to or tolerant toward such parasites. Although an entirely resistant or tolerant variety has not been identified or created thus far (Mohamed et al., 2003; Rubiales, 2003), information on host and non-host responses to parasitic plants has been accumulating at the molecular level. Studies based on the β-glucuronidase (GUS) strategy have revealed that O. aegyptiaca parasitism locally activates genes encoding the following proteins; a basic pathogenesis-related (PR) protein (Joel and Portnoy, 1998), 3-hydroxy-3-methylglutaryl CoA reductase 2 (Westwood et al., 1998), phenylalanine ammonia lyase, chalcone synthase, sesquiterpene cyclase, and farnesyltransferase in Nicotiana tabacum, and 3-hydroxy-3-methylglutaryl CoA reductase 1 in Lycopersicon esculentum (Griffitts et al., 2004). Gowda et al. (1999) used a differential display strategy and isolated 23 genes whose expressions are up-regulated in the roots of Tagetes erecta during invasion by the incompatible S. asiatica. One of these up-regulated genes, i.e., the non-host resistance to S. asiatica (NRSA-1) gene, encodes a protein that is highly homologous to the disease-resistance proteins identified in several plants. Using the suppression subtractive hybridization (SSH) strategy, genes were isolated from Arabidopsis thaliana roots inoculated with O. ramosa (Vieira-Dos-Santos et al., 2003b), Medicago truncatula roots inoculated with O. crenata (Die et al., 2007), and sorghum roots parasitized by S. hermonthica (Hiraoka and Sugimoto, 2008). For each experiment, genes involved in plant defence response mechanisms such as the jasmonic acid (JA) pathway, signal transduction, and cell-wall fortification were isolated.

Recently, Kubo et al. (2008) reported that L. japonicus is a suitable host for the study of parasitism in plants. This model legume is compatible to O. aegyptiaca and incompatible to O. minor, S. gesnerioides, and S. hermonthica, of which only S. hermonthica induces tissue-browning of L. japonicus at the attachment sites. Nearly 700 000 nucleotide sequences representing the Fabaceae are available from the National Center for Biotechnology Information (NCBI) (Graham et al., 2004), and functional genomic studies have been carried out on the model legumes including L. japonicus (VandenBosch and Stacey, 2003). The Institute for Genomic Research (TIGR) has analysed expressed sequence tags (ESTs) from a variety of plant species, including L. japonicus, and clustered the ESTs into tentative consensus sequences (TCs) that represent the minimally redundant set of a species’ expressed genes (http://www.tigr.org/tdb/tgi/ plant.shtml). In this study, two subtracted cDNA libraries were constructed, namely, Lj-Oa and Lj-Sh, by using SSH (Diatchenko et al., 1996). Lj-Oa and Lj-Sh were enriched for L. japonicus genes that were up-regulated in response to parasitism by O. aegyptiaca and S. hermonthica, respectively. Changes in the temporal and systemic expression of the genes were analysed in plants inoculated with O. aegyptiaca and S. hermonthica with the objective of gaining more comprehensive knowledge on both host and non-host responses to parasitic plants at the molecular level.

Materials and methods

Plant materials and growth conditions

Seeds of L. japonicus accession Miyakojima MG-20 were supplied by the National BioResource Project, Miyazaki University, Japan. O. aegyptiaca seeds collected from mature plants parasitizing Vicia sativa were provided by Professor J Scholes, The University of Sheffield, UK. S. hermonthica seeds were obtained from Professor AGT Babiker, Sudan University of Science and Technology, Sudan. L. japonicus plants were grown in rhizotrons as described by Kubo et al. (2008).

Split-root system

For analyses of the systemic gene expression triggered in response to O. aegyptiaca and S. hermonthica parasitism, the split-root system as described by Kosslak and Bohlool (1984) was employed with some modifications. A modified split-root system was developed using two square Petri dishes (height, 14.4 cm; width, 10.4 cm; thickness, 1.6 cm), filled with rockwool, and overlaid with glass fibre paper. This system was carefully designed to prevent any exchange of material between the dishes (Fig. 1).

Fig. 1.
Diagram of the modified split-root assembly. (A), square Petri dishes; (B), glass fibre papers; (C), rockwool; (D), Orobanche aegyptiaca or Striga hermonthica inoculated on one half of the Lotus japonicus roots.

L. japonicus plants grown for 2 weeks in test tubes were transplanted to the modified split-root system, and the roots of each plant were split into halves. The roots placed in one Petri dish were inoculated with O. aegyptiaca and S. hermonthica radicles and those in the other were uninoculated (Fig. 1).

Conditioning and germination of O. aegyptiaca and S. hermonthica seeds and inoculation

The seeds of O. aegyptiaca and S. hermonthica were surface-sterilized and conditioned as described by Kubo et al. (2008) and Sugimoto et al. (2003), respectively. Seed germination was induced using GR24, a synthetic stimulant provided by Professor B Zwanenburg, Nijmegen University, The Netherlands. Radicles of O. aegyptiaca and S. hermonthica were inoculated onto the L. japonicus roots in the manner described by Kubo et al. (2008).

At 10 d and 6 d after inoculation (dai), 10 mm long root segments were excised 5 mm from the inoculation sites of O. aegyptiaca and S. hermonthica, respectively, and were used for SSH. For analyses of the systemic gene expression, 40 radicles each of O. aegyptiaca and S. hermonthica were placed onto the roots in one dish of the modified split-root system at 2 weeks after transplantation. The roots and the leaves in the other uninoculated dish were excised at 1, 2, and 10 dai of O. aegyptiaca and 1, 2, and 6 dai of S. hermonthica. The roots and leaves from uninoculated plants were collected as control samples. The excised roots and leaves were immediately frozen in liquid nitrogen and stored at – 80 °C until use.

Suppression subtractive hybridization (SSH)

Total RNA of L. japonicus was isolated from the O. aegyptiaca-parasitized roots at 10 dai, S. hermonthica-attached roots at 6 dai, and the uninoculated roots using the RNeasy plant mini kit (Qiagen); synthesis of the first and second cDNA strands was performed from 60, 300, and 300 ng total RNA, respectively, using the Clontech SMART PCR cDNA synthesis kit (Clontech). SSH was performed using the Clontech PCR-Select cDNA subtraction kit (Clontech). To construct the Lj-Oa library containing L. japonicus genes up-regulated in response to parasitism by O. aegyptiaca, cDNAs obtained from the O. aegyptiaca-parasitized roots and the uninoculated roots were used as the tester and the driver cDNAs for SSH, respectively. Similarly, to construct the Lj-Sh library containing genes up-regulated in response to parasitism by S. hermonthica, cDNAs obtained from the S. hermonthica-attached roots and the uninoculated roots were used as the tester and the driver cDNAs, respectively. The secondary PCR products were cloned and sequenced and the redundant clones were eliminated as described previously (Hiraoka and Sugimoto, 2008). A database search was performed for each sequence by using the BLASTN, BLASTX, and TBLASTX programs in NCBI and TIGR databases, with E values of ≤1.

Expression analysis of the subtracted cDNAs

The expression of the subtracted cDNAs was analysed by performing quantitative reverse transcriptase-polymerase chain reaction (qRT-PCR) using gene-specific primers designed on the basis of each cDNA sequence. Total RNA was extracted from each sample using the RNeasy plant mini kit. The DNase treatment of each total RNA, cDNA synthesis, and qRT-PCR analysis were performed as described previously (Hiraoka and Sugimoto, 2008). For one qRT-PCR cycle, a cDNA sample equivalent to 0.5 ng of total RNA was used as the template. The values obtained were normalized to those obtained in the case of actin (accession number EU195536), which was used as an internal control and has been confirmed to exhibit similar expression levels under the test conditions. Each experiment was conducted in triplicate. Of the genes isolated by SSH, those exhibiting greater than 2-fold up-regulation were selected by performing qRT-PCR and were deposited in the DNA Data Bank of Japan (DDBJ) database under the accession numbers BB999881 to BB999976.

Results

Isolation of genes up-regulated in response to parasitism by O. aegyptiaca and S. hermonthica and temporal changes in the expression of these genes

O. aegyptiaca tubercle formation and tissue browning at the attachment sites of S. hermonthica, as reported by Kubo et al. (2008), were observed on L. japonicus roots at 10 dai and 6 dai, respectively. These roots were employed in SSH for constructing the subtracted cDNA libraries Lj-Oa and Lj-Sh. Lj-Oa and Lj-Sh comprised 297 and 336 colonies, respectively, containing the PCR product inserts. After eliminating redundancy, 116 Lj-Oa colonies and 89 Lj-Sh colonies were selected. The expression levels of all the Lj-Oa genes in O. aegyptiaca-parasitized roots and uninoculated roots were compared by performing qRT-PCR, and 48 genes that exhibited greater than 2-fold up-regulation were identified as Orobanche-induced genes. Similarly, 48 Lj-Sh genes were identified as Striga-induced genes. No overlapping nucleotide sequence was detected in the Orobanche- and the Striga-induced genes.

Temporal changes in the expression levels of the Orobanche-induced genes in the L. japonicus roots were evaluated at 1, 2, and 10 dai. Similarly, the expression levels of the Striga-induced genes in the roots were evaluated at 1, 2, and 6 dai. On the basis of the expression at 1 dai, all the genes were classified into three clusters as shown in Figs 2 and and3.3. Clusters I, II, and III comprised genes that exhibited up-regulation, constant expression, and down-regulation, respectively, at 1 dai. Of the Orobanche-induced genes, 19, 26, and 3 genes were classified into clusters I, II, and III, respectively (Fig. 2). On the other hand, 6, 33, and 9 of the Striga-induced genes were classified into these respective clusters (Fig. 3). Of the genes in cluster I, the expression levels of 11 Orobanche-induced genes and three Striga-induced genes were similar to those in uninoculated roots at 2 dai (Figs 2, ,3),3), and those in LjOa116-3s and LjOa25 exhibited transient down-regulation at 2 dai (Fig. 2). In the clusters II and III, the expression of most Orobanche- and Striga-induced genes was up-regulated only at 10 and 6 dai, respectively (Figs 2, ,33).

Fig. 2.
Expression profiles of Lotus japonicus genes that were up-regulated in response to Orobanche aegyptiaca parasitism, as determined by performing quantitative RT-PCR. Clusters I, II, and III include genes that were up-regulated, constantly expressed, and ...
Fig. 3.
Expression profiles of Lotus japonicus genes that were up-regulated in response to Striga hermonthica attachment as determined by performing quantitative RT-PCR. Clusters I, II, and III include genes that were up-regulated, constantly expressed, and down-regulated, ...

Functional categories of up-regulated genes

On the basis of their functions suggested by the homology search, all the Orobanche- and Striga-induced genes were classified into 11 categories (Tables 1, ,2).2). JA biosynthesis- and phytoalexin biosynthesis-related genes were exclusively included in Lj-Oa and Lj-Sh, respectively (Tables 1, ,2).2). The JA biosynthesis-related genes LjOa25, LjOa83-1, and LjOa74 were found to be homologous to the lipoxygenase (LOX)-encoding genes of Pisum sativum, Cicer arietinum, and Sesbania rostrata, respectively (Table 1). Further, the phytoalexin biosynthesis-related genes LjSh207, LjSh46-1, and LjSh29s were identical to those encoding isoflavone reductase (IFR), pinoresinol-lariciresinol reductase (PLR), and cytochrome P450 in L. japonicus, respectively (Table 2).

Table 1.
Genes showing up-regulated expression in the roots of Lotus japonicus after 10 d of Orobanche aegyptiaca inoculation
Table 2.
Genes showing up-regulated expression in the roots of Lotus japonicus after 6 d of Striga hermonthica inoculation

Seven genes involved in nodulation were included among the Orobanche-induced genes (Table 1). Both LjOa198 and LjOa85s were found to be homologous to a lectin-encoding gene of Lotus tetragonolobus. LjOa51-2 was identified as a gene encoding Nod factor-binding lectin-nucleotide phosphohydrolase (LNP). LjOa95, LjOa60-1, LjOa157-1, and LjOa109 were determined to be homologous to the repetitive proline-rich cell-wall protein (PRP) 2 precursor of M. truncatula, the MtN19-like protein of P. sativum, actin-depolymerizing factor 2 of Petunia hybrida, and an EST generated from the nodules of 5- and 7-week-old L. japonicus plants, respectively (Table 1). The Striga-induced genes included only one gene involved in nodulation.

In the case of PR genes, nine out of the 15 in the Orobanche-induced genes were homologous to protease-inhibitor genes (Table 1). On the other hand, only one protease-inhibitor gene was included among the Striga-induced genes (Table 2).

Systemic expression of up-regulated genes

Genes were selected that exhibited greater than 8-fold up-regulation at either time point after the inoculation of O. aegyptiaca or S. hermonthica (Figs 4A, ,5A),5A), and their systemic expression was analysed (Figs 4B, 5B, 5C). Among 16 Orobanche-induced genes, four genes, namely, LjOa9, LjOa116-3s, LjOa169, and LjOa147-2 exhibited greater than 8-fold up-regulation at 10 dai (Fig. 5B). The expression of these four genes in the leaves was also analysed, and a 10-fold up-regulation of LjOa9 expression was detected at 10 dai (Fig. 5C). Similarly, the systemic expression of 14 genes selected from among the Striga-induced genes was analysed in the uninoculated roots at 1, 2, and 6 dai (Fig. 4B). However, no gene exhibited significant up-regulation (Fig. 4B).

Fig. 4.
Local (A) and systemic (B) expression of the 12 Orobanche-induced genes and the 14 Striga-induced genes in Lotus japonicus roots. The x-axis indicates the clone number and the days after inoculation of each gene. The y-axis indicates fold expression induction ...
Fig. 5.
Local expression (A) and systemic expression (B) in Lotus japonicus roots, and systemic expression (C) in L. japonicus leaves of the four Orobanche-induced genes. The x-axis indicates the clone number and the days after inoculation of each gene. The ...

Discussion

The fact that no overlapping nucleotide sequence was detected between the Orobanche-induced genes and Striga-induced genes indicates that L. japonicus roots are able to distinguish the compatible parasite from the incompatible one. The expression of most of the Striga-induced genes in the inoculated roots was as low as that in the uninoculated roots at 1 dai and 2 dai. This delayed response is consistent with the phenomena of tissue browning, which was not observed at 1 dai or 2 dai but was evident at 6 dai of S. hermonthica (Kubo et al., 2008). On the other hand, the expression of approximately 40% (19 genes) of the Orobanche-induced genes was up-regulated at 1 dai of O. aegyptiaca. Considering that 13 out of the 19 genes exhibited up-regulation at 1 dai and 10 dai and down-regulation at 2 dai, the expression of these 13 genes may, therefore, have been induced at different stages of parasitism, namely, attachment and tubercle formation. These results are in accord with those of a previous study by Vieira-Dos-Santos et al. (2003b), wherein four out of the 13 Arabidopsis genes that were up-regulated by O. ramosa parasitism exhibited a second induction phase at 7 dai.

Genes encoding putative LOX were exclusively included among the Orobanche-induced genes. LOX oxidizes linolenic acid, and the resultant hydroperoxide can be a precursor of JA (Liechti and Farmer, 2002). Previous reports have also described the induction of genes related to JA biosynthesis in host plants parasitized by O. ramosa (Vieira-Dos-Santos et al., 2003a, b), O. crenata (Die et al., 2007), and S. hermonthica (Hiraoka and Sugimoto, 2008). It is well-known that JA mediates wound responses in plants (Mason and Mullet, 1990). Up-regulation of LOX gene expression is indicative of host root wounding by the parasite and the stress signal is transmitted via JA although it dose not elicit a rapid response (Fig. 2). This hypothesis is supported by a light microscopic study conducted by Kubo et al. (2008), which revealed that the O. aegyptiaca endophyte oppresses the L. japonicus vascular parenchyma, xylem, and phloem.

Interestingly, attachment of the incompatible S. hermonthica to the host roots induced the specific expression of genes encoding IFR, PLR, and cytochrome P450, which catalyse the late steps in the biosynthesis of vestitol, a legume-specific phytoalexin 5-deoxyisoflavonoid (Shimada et al., 2007). Vestitol accumulates in L. corniculatus in response to inoculation with the fungus Helminthosporium turcicum (Bonde et al., 1973). Induction of vestitol biosynthesis-related genes suggests that L. japonicus recognizes the incompatible S. hermonthica as an unfavourable intruder similar to pathogenic fungi, and it then synthesizes vestitol as a non-host resistance response to S. hermonthica. In a study on the response of M. truncatula to O. crenata, Lozano-Baena et al. (2007) demonstrated that phenolic compounds accumulate in infected host roots; however, neither the chemical structures nor the biological functions of these compounds have been identified to date. The above-mentioned authors postulated that the host poisons the parasite by releasing toxic metabolites through the vascular connections.

The fact that the genes involved in nodulation were almost exclusively found among the Orobanche-induced genes suggests that L. japonicus recognizes the compatible O. aegyptiaca as a symbiont similar to rhizobium. Among the seven nodulation-related genes, the putative lectin genes (LjOa198 and LjOa85s) and LNP (LjOa51-2) exhibited up-regulation at 1 dai. In Dolichos bifrorus, Db-LNP, which is expressed on the surface of young and emerging root hairs, binds to the Nod factors produced by rhizobial strains that nodulate this plant (Roberts et al., 1999). Db-LNP is redistributed to the tips of the root hairs in response to root treatment with a rhizobial symbiont or with the Nod factor but not with a non-symbiotic rhizobial strain or a root pathogen (Kalsi and Etzler, 2000). The expression of LjOa95, which is homologous to MtPRP2, was also induced at 1 dai. MtPRP2 is important for remodelling of the host extracellular matrix, which is involved in the early response of legume host roots to rhizobia (Wilson et al., 1994). The four genes that exhibited up-regulated expression at 1 dai may play significant roles during the early stages of the parasitic establishment of O. aegyptiaca.

It is noteworthy that PR genes accounted for 31% of the Orobanche-induced genes and that more than half of the PR genes were up-regulated at 1 dai. In another compatible relationship between sorghum and S. hermonthica, wherein the tubercle formation rate was high (>58%), only two PR genes were included among the 30 genes that were up-regulated by parasitism (Hiraoka and Sugimoto, 2008). A low rate of tubercle formation (<10%) may be attributable to the up-regulation of PR gene expression in L. japonicus following O. aegyptiaca attachment.

The phenomena of systemic induction of genes in response to plant parasitism are disputable. Gowda et al. (1999) reported that S. asiatica infection induces the systemic expression of NRSA-1 in the roots and leaves of T. erecta. On the other hand, no systemic gene induction was detected in N. tabacum and L. esculentum parasitized by O. aegyptiaca (Joel and Portnoy, 1998; Westwood et al., 1998; Griffitts et al., 2004). However, in the present study, it was observed that O. aegyptiaca parasitism induced the systemic expression of LjOa9, which is homologous to a miraculin-like protein; this demonstrated that wound-induced signal transduction was systemically induced in L. japonicus by O. aegyptiaca parasitism.

In summary, the L. japonicus genes that are up-regulated in response to parasitism by the compatible species O. aegyptiaca and the incompatible species S. hermonthica were isolated. Our comparison between the Orobanche- and the Striga-induced genes with regard to their expression patterns and putative functions suggested that L. japonicus is likely to recognize the incompatible species S. hermonthica as an unfavourable intruder. Moreover, Nod genes were induced following the attachment of the compatible species O. aegyptiaca to the host roots. Successful parasitism induced the expression of JA and PR genes, some of which were systemically expressed.

Acknowledgments

The authors thank Ms Ayaka Hamasaki and Ms Miho Sugo for their technical assistance in various aspects of the study. This work was supported, in part, by a Grant-in-Aid for Scientific Research (B) (Nos 17405027 and 20405026), by a grant from the AA Science Platform Program of the Japan Society for the Promotion of Science, and by a grant from the Sumitomo Foundation to YS.

Glossary

Abbreviations

dai
day(s) after inoculation
EST
expressed sequence tag
GUS
β-glucuronidase
IFR
isoflavone reductase
JA
jasmonic acid
LAR
localized acquired resistance
LNP
Nod factor-binding lectin-nucleotide phosphohydrolase
LOX
lipoxygenase
MeJA
methyl jasmonate
PLR
pinoresinol-lariciresinol reductase
PR protein
pathogenesis-related protein
PRP
proline-rich cell-wall protein
qRT-PCR
quantitative reverse transcriptase-polymerase chain reaction
SA
salicylic acid
SSH
suppression subtractive hybridization

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