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Update on Microbial Interactions and Plant Defense

Recent Advances in Legume-Microbe Interactions: Recognition, Defense Response, and Symbiosis from a Genomic Perspective¹

United States Department of Agriculture-Agricultural Research Service Plant Science Research Unit, St. Paul, Minnesota 55108 (D.A.S.); Department of Plant Pathology, University of Minnesota, St. Paul, Minnesota 55108 (D.A.S.); United States Department of Agriculture-Agricultural Research Service Corn Insects and Crop Genetics Research Unit, Ames, Iowa 50011 (M.A.G.); and Department of Agronomy, Iowa State University, Ames, Iowa 50011 (M.A.G.)

The ability of legumes to form symbiotic mutualistic relationships with certain bacteria in the Rhizobiales (collectively called rhizobia) and harness the ability of the bacteria to fix atmospheric N₂ into ammonia has a tremendous impact on natural and agricultural ecosystems. The interaction enables legumes to produce protein-rich seeds and foliage that are critical to many human and animal diets. Past research has illuminated many of the facets of plant-bacterium recognition, nodule formation, nitrogen fixation, and ammonia assimilation. Less well understood are the mechanisms that allow bacterial colonization without triggering plant defense responses. Specifically, how do legumes recognize friend from foe? Recent genomic research probing legume-pathogen and legume-rhizobial interactions are providing clues to help answer this question. Of particular interest are the roles of flavonoid compounds in legume-rhizobial and legume-pathogen interactions. Legumes are a rich source of flavonoids, notably the isoflavones and isoflavanones, which are not found in Arabidopsis (Arabidopsis thaliana). Legume nodules are also rich sources of Cys cluster proteins (CCPs), some of which have been shown to have antimicrobial activity and may play a role in protecting nodules from pathogens. This Update will summarize recent information on molecular characterization of legume disease resistance (R) genes, R-gene-mediated interactions with pathogens, and parallels in legume-rhizobial interactions.

	ROLE OF R GENES AND RECEPTORS IN LEGUME-MICROBE INTERACTIONS

TOP ROLE OF R GENES... IDENTIFYING R-GENE-MEDIATED AND... MULTIPLE ROLES OF FLAVONOID... ANALYSIS OF ESTS IDENTIFIES... CONCLUSION LITERATURE CITED

 
While over 40 disease R genes have been isolated from plants (Martin et al., 2003), only two have been isolated from a legume. Isolation of R genes from legumes has been slow due to lack of detailed genetic maps, appropriate mapping populations, and chromosome walking tools. In addition, the polyploid genomes of many crop legumes makes obtaining mutants difficult, and high frequency transformation systems for legumes are limited. With the active development of genetic and genomic tools for model and crop legumes, isolation of more legume R genes should be forthcoming. Numerous R gene homologs have been identified in legume species by sequence identity of conserved motifs with known R genes (Kanazin et al., 1996; Yu et al., 1996; Zhu et al., 2002). The challenge is to identify the specific genes conferring resistance to a particular pathogen.

The Rpg1-b gene from soybean (Glycine max) confers resistance to Pseudomonas syringae pv glycinea (causing bacterial blight) carrying the avrB gene in a classic gene-for-gene specific manner (Ashfield et al., 2004). The Rpg1-b gene is a member of the coiled-coil nucleotide-binding Leu-rich repeat (CC-NB-LRR) class of R genes. Interestingly, it shares only limited sequence similarity with the Arabidopsis RPM1 gene, which also confers resistance to P. syringae expressing avrB. Phylogenetic analysis demonstrated that Rpg1-b and RPM1 are not orthologous, suggesting that R genes with avrB specificity have arisen at least twice during plant evolution.

Isolation of four highly similar CC-NB-LRR genes from the Rps1-k locus of soybean conferring resistance to the oomycete pathogen Phytophthora sojae, the causal agent of Phytophthora root and stem rot, suggests a recent duplication event (Gao et al., 2005). Of the four CC-NB-LRR-type R genes identified, three (Rps1-k-1, Rps1-k-3, and Rps1-k-4) have identical open reading frames. The Rps1-k-2 gene shares 89.9% amino acid identity to the other three genes. The 3' untranslated region of Rps1-k-3 appears to have arisen from a recombination event between the 3' ends of the two gene classes. Three genes (Rps1-k-1, Rps1-k-2, and Rps1-k-3) representing the two classes were shown to confer resistance to P. sojae. The R genes from the Rps1-k locus are unique because they are the only identical R genes identified from the same haplotype in plants. There are many additional members of the gene family in the Rps1 region and it is possible that additional paralogs of Rps1-k-2 may be located adjacent to the Rps1-k locus. Further investigation of these genes and additional R genes from other legumes will increase our understanding of R gene evolution and function.

Characterization of R genes has focused on plant interactions with pathogens. However, the possibility of R genes mediating interactions with other microbes, including symbionts, cannot be discounted. In soybean, the Rj2 locus, causing an ineffective nodulation phenotype, is clustered in the genome with resistance to P. sojae and powdery mildew. Sequencing of the corresponding 120 kb region in a nodulating genotype found no evidence of known nodulation genes. Instead, the region was composed almost entirely of R genes, with 16 different TIR-NB-LRR R genes (Graham et al., 2002). As in the case of the Rps1-k locus, evidence of duplication and unequal recombination exists. These findings suggest that R genes may also be involved in recognizing beneficial symbionts.

Gene-for-gene responses are based on recognition of avirulence or effector proteins produced by pathogens or the effect of these proteins on targets within plant cells. The effector proteins of gram-negative plant pathogenic bacteria are delivered to cells by a type three secretion system (TTSS). Sequencing of rhizobial plasmids and chromosomes revealed a TTSS in some, but not all species (Marie et al., 2001). Thus, a TTSS is not a requirement for symbiosis. A number of proteins termed nodulation outer proteins (Nops) are delivered via the TTSS (Marie et al., 2003). In interactions with some hosts Nops act somewhat like virulence factors, while in other potential hosts they appear to act like avirulence factors by triggering a rapid defense response against the bacterium. Some effectors from plant pathogenic bacteria suppress plant defense responses. To investigate the function of NopL, Bartsev et al. (2004) expressed nopL in tobacco (Nicotiana tabacum) plants. When these plants were inoculated with Potato virus Y, expression of the defense proteins class I chitinase and -1,3-glucanase was suppressed and virus accumulation was enhanced. Similarly, expression of nopL in transgenic Lotus japonicus plants also suppressed accumulation of class I chitinase. Whether Nop proteins trigger host defenses in a gene-for-gene manner, the structure of such a host gene and the components of the signal transduction cascade remain to be discovered.

The cascade of plant responses leading to nodule formation is triggered by recognition of bacterially produced lipo-chitooligosaccharide Nod factors by a family of LysM receptor kinases. Thus far, five LysM receptor kinases have been identified that mediate Nod factor recognition, including NFR1 (Radutoiu et al., 2003) and NFR5 (Madsen et al., 2003) from L. japonicus and NFP (Arrighi et al., 2006), LYK3, and LYK4 (Limpens et al., 2003) from Medicago truncatula. While Ser-Thr receptor kinases are ubiquitous, the addition of LysM domains is quite rare. Zhu et al. (2006) identified orthologs of the legume LysM receptor kinases from rice (Oryza sativa) and Arabidopsis. Sequence similarity and synteny studies confirmed these nonlegume orthologs, however their function remains unknown. Recent evidence suggests LysM domains may also be involved in pathogen recognition. Kaku et al. (2006) identified a rice chitin oligosaccharide elicitor binding protein with two LysM domains.

	IDENTIFYING R-GENE-MEDIATED AND BASAL DEFENSES BY TRANSCRIPT PROFILING

TOP ROLE OF R GENES... IDENTIFYING R-GENE-MEDIATED AND... MULTIPLE ROLES OF FLAVONOID... ANALYSIS OF ESTS IDENTIFIES... CONCLUSION LITERATURE CITED

 
Large-scale transcript profiling of soybean and M. truncatula has been used to identify genes expressed in R-gene-mediated incompatible plant-microbe interactions, leading to disease resistance and compatible interactions, in which basal defense responses are expressed but disease occurs. All incompatible interactions and some compatible interactions were characterized by strong, rapid up-regulation of genes encoding enzymes in the phenylpropanoid pathway, particularly for synthesis of isoflavones and isoflavanones. These experiments also identified additional defense responses, some of which may be novel, utilizing genes not previously characterized.

The responses of the soybean ‘Williams 82’ to avirulent and virulent strains of the bacterial pathogen P. syringae pv glycinea, differing in the presence or absence of avrB, were investigated using a 27,648 cDNA array (Zou et al., 2005). Only 45 genes were specific to the susceptible response. In contrast, over 2,000 genes were differentially expressed uniquely in the resistant response at 8 h after inoculation (hai) and over 1,000 genes at 24 hai. Many of these genes are involved in plant processes previously shown to respond to biotic and abiotic stresses. However, a large proportion had unknown function. Of particular interest was the down-regulation of chloroplast-associated genes and genes specific to the anthocyanin branch of the phenylpropanoid pathway. The authors suggest that chloroplasts play a key role in hypersensitive response (HR)-mediated resistance responses. Specifically, PSII appears to be a major source of the oxidative burst specific to the HR. Destruction of the D1 subunit of PSII leads to photooxidation and formation of reactive oxygen species, which are detrimental to the pathogen. Down-regulation of chloroplast-associated genes is likely in response to the altered redox state of the cell from the oxidative burst and high levels of reactive oxygen species. Dominating the up-regulated genes were genes in the flavone and isoflavone branches of the phenylpropanoid pathway (Zabala et al., 2006). Accumulation of these transcripts was observed in both susceptible and resistant responses, although a higher fold change was associated with resistance. Accumulation of transcripts in this pathway and the concomitant down-regulation of genes in the anthocyanin pathway are suggested to enhance production of isoflavones, which can act as antioxidants and have antimicrobial activity.

Response of soybean to the fungal pathogen Fusarium solani f. sp. glycines, the causal agent of sudden death syndrome (SDS), was followed in the susceptible ‘Essex’ and a partially resistant recombinant inbred line (RIL23) carrying six quantitative trait loci for resistance to SDS (Iqbal et al., 2005). In RIL23 at 3, 7, and 10 d after inoculation, a total of 81, 88, and 129 genes were up-regulated 2-fold or more, respectively. Little change occurred in the susceptible genotype compared to the mock-inoculated control. A sustained up-regulation of several genes encoding enzymes in the phenylpropanoid pathway was observed in RIL23 over the 10 d time period and implicates the products of the pathway in resistance to SDS.

Transcript profiling of the susceptible response of soybean to the oomycete pathogen P. sojae was followed from 3 to 48 hai (Moy et al., 2004). In total, 8% of the genes were up-regulated 2-fold or more and 5% were down-regulated. Changes in transcript abundance in response to the pathogen were rapid. At 3 hai 22 genes were up-regulated 2-fold or more and at 6 hai 97 genes were similarly up-regulated. Among the up-regulated genes at 6 hai were enzymes of phenylpropanoid metabolism, oxidative stress, and pathogenesis-related (PR) protein 1a. From 12 to 48 hai there was a sustained transcript accumulation of genes encoding enzymes of phytoalexin metabolism, defense, and signaling proteins. In contrast, genes involved in terpenoid metabolism showed no change or were down-regulated. Specific peroxidase and lipoxygenase genes were among the most strongly down-regulated. It is unclear whether up-regulation of the isoflavonoid pathway in this susceptible interaction was related to necrosis of plant tissue in response to the pathogen or was a component of basal defense responses. Isoflavones have been shown to be important in R-gene-mediated resistance to P. sojae. Down-regulating isoflavone synthase genes in soybean roots using an RNAi approach resulted in a >95% reduction in isoflavone accumulation and an enhanced susceptibility to the pathogen (Subramanian et al., 2005).

Interestingly, in susceptible soybean roots (‘Kent’) inoculated with the soybean cyst nematode, a biotrophic pathogen, defense response genes or genes in the flavonoid pathway were differentially expressed only during early time points (6 hai; Alkharouf et al., 2006). Expression of these genes may be in response to wounding caused by nematode invasion. Expression profiles at later time points are dominated by genes involved in primary metabolism, cell structure, and protein synthesis, all of which are needed for establishing nematode feeding sites. Because isoflavonoid phytoalexins are associated with resistance to soybean cyst nematode (Huang and Barker, 1991), in the compatible interaction the nematode may not trigger defenses or may actively suppress host defense responses. In L. japonicus, inoculation with root knot nematode (Meloidogyne spp.) induces root hair deformation and branching, morphologically and cytologically identical to that induced by rhizobial Nod factors (Weerasinghe et al., 2005). This reaction was not seen in nfr1, nfr5, or symRK mutants defective in Nod factor signaling. This suggests the nematode produces a compound functionally equivalent to Nod factor that interacts with these receptors, allowing the nematode to escape defense responses.

Sustained up-regulation of genes involved in phenylpropanoid metabolism has been associated with R-gene-mediated resistance responses in M. truncatula responding to foliar pathogens. Expression profiling was carried out from 16 to 72 hai with the fungal pathogen Colletotrichum trifolii in leaves of a susceptible and resistant genotype (Torregrosa et al., 2004). At 16 hai, both genotypes responded to infection by up-regulation of genes for PR proteins, lipoxygenases, cell wall proteins, and phenylpropanoid pathway enzymes. Transcript accumulation of the majority of these genes remained elevated from 24 to 72 hai in the resistant line. In contrast, transcripts dropped to baseline amounts or were down-regulated in the susceptible line. In the resistant line among the most highly up-regulated were genes for oxylipin synthesis, isoflavonoid synthesis, PR10 proteins, and several proteins previously thought to be specific to nodules. The strong up-regulation of lipoxygenase genes in the resistant line suggests involvement of the oxylipin pathway and jasmonic acid signaling in the resistant response.

Transcript profiling of M. truncatula responding to a biotrophic pathogen, Erysiphe pisi, the causal agent of powdery mildew, identified genes potentially involved in basal defense and the HR (Foster-Hartnett et al., 2007). In a resistant, moderately resistant, and susceptible genotype, up-regulation of genes was observed for PR proteins, particularly many PR10 family members, PR1, EDS1, glutathione S-transferase, and -1,3-glucanase. Expression of the latter four genes implicates salicylic acid responses in the basal response to this pathogen. Down-regulation of a wide range of genes was also observed, including genes involved in primary metabolism, stress response, signaling proteins, lipid metabolism, and genes with unknown function. Specific to the resistant HR was up-regulation of genes in the phenylpropanoid pathway, particularly those leading to isoflavone and isoflavonoid compounds, several transcription factors, and a large number of genes of unknown function, including several genes specific to legumes.

Legumes are a rich source of several subclasses of PR-10 proteins, some with ribonuclease and antifungal activity (Bantignies et al., 2000; Chadha and Das, 2006). Interestingly, Arabidopsis does not appear to express PR-10-like proteins. Up-regulation of genes with similarity to the parsley (Petroselinum crispum) PR-10 gene, MtN13, and early nodulins 12A and 12B, occurred specifically in the resistant interaction of M. truncatula with E. pisi (Foster-Hartnett et al., 2007). Previously, these genes were described as nodule limited in expression (Scheres et al., 1990; Gamas et al., 1998). Up-regulation of specific PR-10 genes was also observed in the resistant interaction of M. truncatula with C. trifolii (Torregrosa et al., 2004). Although PR-10-like proteins accumulated in M. truncatula roots after inoculation with the oomycete pathogen Aphanomyces eutiches, the proteins were associated with a susceptible reaction (Colditz et al., 2005). The high transcript abundance after pathogen inoculation and in vitro activity of PR-10 proteins suggests that these proteins play a key role in legume-microbe interactions.

	MULTIPLE ROLES OF FLAVONOID COMPOUNDS IN LEGUME-RHIZOBIAL INTERACTIONS

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Flavonoid compounds, particularly isoflavonoids, are key components in defense responses of legumes to pathogens in which they likely have roles in restricting microbial growth and as antioxidants. However, many of the same compounds also play key roles in establishing an effective symbiotic mutualism with rhizobia. Research has shown that flavonoid compounds are responsible for initiation of legume-rhizobial interactions and influence many of the events needed for successful root infections by rhizobia (for review, see Cooper, 2004). Flavonoid compounds attract rhizobia to host roots, stimulate growth, modify composition of bacterial cell wall components, induce expression of nod genes leading to production of Nod factors, induce expression of the TTSS, and induce expression of plant cell wall degrading enzymes.

Transcript profiling of M. truncatula roots following inoculation with Sinorhizobium meliloti suggests that phenylpropanoid pathway genes and defense-response genes are highly regulated in the infection process. Using a 6,000 cDNA microarray, transcript accumulation was measured in roots from 1 to 72 hai (Lohar et al., 2006). Up-regulation of defense- and stress-response genes was observed at 1 hai, suggesting rapid recognition of the symbiont by the host plant. However, at 6 hai and thereafter, these genes were down-regulated. As a functional category, genes involved in flavonoid biosynthesis were up-regulated at 6 hai and thereafter. However, not all gene family members had the same transcript accumulation pattern. Some members of the chalcone synthase family were up-regulated from 6 to 72 hai compared to control roots, while others were up-regulated transiently, and some were down-regulated. The specificity of down-regulation of defense responses and particular genes involved in phenylpropanoid biosynthesis and whether regulation is due to bacterial or plant signals is yet to be determined.

After initial nodule formation, the host inhibits additional rhizobial infections to limit nodule number. In landmark research, Vasse et al. (1993) showed that an HR-like response occurs in alfalfa (Medicago sativa) root cells with aborted infection threads and that the necrotic cells contain fluorescent phenolic compounds and enzymes of the phenylpropanoid pathway. Recent research using an alfalfa split root system provides evidence for systemic suppression of nod gene-inducing flavonoid compounds after initial nodulation as a means of inhibiting new infections (Catford et al., 2006). The split root system was also used to demonstrate that Nod factor treatment inhibits arbuscular mycorrhizal symbiosis (Catford et al., 2003). It is unclear how modulation of flavonoids and other defense responses after nodulation may affect defenses against pathogens. Systemic defense responses are not well characterized in legumes and this topic warrants further investigation to determine how systemic acquired resistance impacts nodulation. Inhibiting production of salicylic acid, which plays a key role in inducing the HR and in systemic acquired resistance, increases nodulation in L. japonicus and M. truncatula (Stacey et al., 2006), suggesting that SA-induced defenses are also involved in controlling nodulation.

	ANALYSIS OF ESTS IDENTIFIES GENES INVOLVED IN NODULATION AND DEFENSE

TOP ROLE OF R GENES... IDENTIFYING R-GENE-MEDIATED AND... MULTIPLE ROLES OF FLAVONOID... ANALYSIS OF ESTS IDENTIFIES... CONCLUSION LITERATURE CITED

 
Prior to microarray analyses and whole-genome sequencing, ESTs provided a mechanism to identify genes expressed during nodulation or defense. Fedorova et al. (2002) analyzed the M. truncatula ESTs to identify genes specific to nodulation. Of the 340 nodule-specific sequences identified, 114 encoded nodule-specific CCPs, whose function was unknown. Graham et al. (2004) identified more than 300 nodule- and seed-specific CCPs from M. truncatula and 20 seed-specific CCPs from soybean, while trying to identify legume-specific sequences from EST data. Motif analyses of the CCPs revealed similarity to plant defensins. Like defensins, the CCPs could be characterized by a conserved signal peptide, a highly divergent mature peptide with the exception of conserved Cys residues, and tissue-specific expression. Using CCP motif models developed from M. truncatula and soybean, Silverstein et al. (2005) identified >300 defensin-like genes in the Arabidopsis genome. Genome analyses revealed that plant defensins had many features of classical R genes including clustering and evolution by duplication and positive selection. Why are so many defensin-like sequences needed in the nodule? Graham et al. (2004) proposed that nodule-specific CCPs protect the carbon-rich nodule from pathogen attack. The defense response would inhibit pathogen attack, while allowing the legume-rhizobial mutualism to occur. Purified protein extracts of two nodule-specific CCPs have antimicrobial activity against P. syringae and Clavibacter michiganensis but no affect on the growth of the S. meliloti (M. Graham, unpublished data).

EST data can also be used to identify genes important in nodulation and defense. Silverstein et al. (2005) and Graham et al. (2006) used Fisher exact tests to identify EST contigs (from the Institute for Genomic Research, www.tigr.org) that were statistically overrepresented with ESTs from particular cDNA libraries. Using the same approach, we identified M. truncatula and soybean cDNA contigs that were statistically overrepresented (P < 0.05) with ESTs from at least two different pathogen or rhizobia-inoculated libraries. Of the 4,588 contigs identified from soybean, 65% were specific to defense, 27% were specific to nodulation, and 8% were expressed during nodulation and defense. In M. truncatula, 4,877 contigs were identified; 51% were specific to defense, 37% were specific to nodulation, and 12% were expressed in symbiont- and pathogen-inoculated libraries (M. Graham, unpublished data). Of particular interest was a group of GRAS transcription factors overrepresented with ESTs from either symbiont- or pathogen-inoculated libraries. The GRAS family of transcription factors has roles in root development and signaling (Bolle, 2004). Two GRAS family members from M. truncatula, NSP1 (Smit et al., 2005) and NSP2 (Kaló et al., 2005), are required for Nod factor signaling. In contrast, CIGR1 and CIGR2 from rice are induced by N-acetylchitooligosaccharide elicitor perception (Day et al., 2003) and GRAS genes are important for disease resistance in tomato (Solanum lycopersicum;Mayrose et al., 2006). These findings again suggest that the symbiosis and defense pathways overlap and many genes with roles in mutualism and defense are waiting to be discovered.

	CONCLUSION

TOP ROLE OF R GENES... IDENTIFYING R-GENE-MEDIATED AND... MULTIPLE ROLES OF FLAVONOID... ANALYSIS OF ESTS IDENTIFIES... CONCLUSION LITERATURE CITED

 
The emerging picture from recent research indicates that legumes utilize similar mechanisms to recognize pathogens and symbiotic microbes. Work from several labs suggests that LysM domains and GRAS transcription factors are important for recognition of both friend and foe. Both rhizobia and successful pathogens suppress plant defenses to establish an infection. Later in the rhizobial interaction, however, specific plant defense responses are important in nodule development and protection. Isoflavonoid compounds are important in halting infection by pathogens and rhizobia and in controlling nodule number. Defensin-like genes appear to protect the nodule from pathogen attack. Clearly, we are on the verge of understanding how these two complex pathways interact. Microarray technologies will allow us to identify genes acting in both symbiosis and defense. However, we are still limited by the time and effort required to functionally characterize candidate genes.

	ACKNOWLEDGMENTS

 
We regret that due to space limitations, we could not include all recent legume-microbe interaction research articles.

Received February 1, 2007; accepted March 6, 2007; published June 6, 2007.

	FOOTNOTES

 
¹ This work was supported by the National Science Foundation Plant Genome Project (award no. 0110206).

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: Deborah A. Samac (dasamac{at}umn.edu).

www.plantphysiol.org/cgi/doi/10.1104/pp.107.096503

^* Corresponding author; e-mail dasamac{at}umn.edu; fax 651–649–5058.

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