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Srsymrk, a Plant Receptor Essential for Symbiosome Formation

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Srsymrk, a Plant Receptor Essential for Symbiosome Formation SrSymRK, a plant receptor essential for symbiosome formation Ward Capoen*, Sofie Goormachtig*, Riet De Rycke, Katrien Schroeyers, and Marcelle Holsters† Department of Plant Systems Biology, Flanders Interuniversity Institute for Biotechnology, Ghent University, Technologiepark 927, B-9052 Ghent, Belgium Communicated by Marc C. E. Van Montagu, Ghent University, Ghent, Belgium, May 23, 2005 (received for review March 31, 2005) The symbiosis between legumes and rhizobia is essential for the domains bind peptidoglycan or chitin (10, 11); hence, plant nitrogen input into the life cycle on our planet. New root organs, LysM-receptor-like kinases are good candidates for NF binding the nodules, are established, which house N2-fixing bacteria inter- and perception. nalized into the host cell cytoplasm as horizontally acquired or- In addition, other NF signal transduction elements act down- ganelles, the symbiosomes. The interaction is initiated by bacterial stream from the LysM-receptor-like kinases, because the cor- invasion via epidermal root hair curling and cell division in the responding mutants still respond to NFs by root hair swelling, but cortex, both triggered by bacterial nodulation factors. Of the no longer show a root hair curling (RHC) response. In Medicago several genes involved in nodule initiation that have been identi- truncatula, the Dmi1, Dmi2, and Dmi3 (12) genes encode a fied, one encodes the leucine-rich repeat-type receptor kinase putative ligand-gated cation channel, a leucine-rich repeat SymRK. In SymRK mutants of Lotus japonicus or its orthologs in (LRR)-type receptor kinase, and a putative calcium and cal- Medicago sp. and Pisum sativum, nodule initiation is arrested at the modulin-dependent protein kinase, respectively (13–15). Or- level of the root hair interaction. Because of the epidermal block, thologs of Dmi2 have been described in M. sativa (MsNork), the role of SymRK at later stages of nodule development remained Lotus japonicus (LjSymRK), and Pisum sativum (Pssym19) (13, enigmatic. To analyze the role of SymRK downstream of the 16). Remarkably, mutations in these genes also impair arbuscu- epidermis, the water-tolerant legume Sesbania rostrata was used lar mycorrhization, which is an ancient and widespread endo- that has developed a nodulation strategy to circumvent root hair symbiosis that facilitates phosphate acquisition and involves 80% responses for bacterial invasion. Evidence is provided that SymRK of the land plants and fungi belonging to the Glomeromycota plays an essential role during endosymbiotic uptake in plant cells. (17). Hence, the pathways of nodulation and mycorrhization share common genetic elements for the establishment of endo- bacterial uptake ͉ endosymbiosis ͉ legume nodulation ͉ Sesbania symbiotic structures (17). Recently, a nonsymbiotic, NF- rostrata ͉ infection thread structure independent phenotype of enhanced touch sensitivity has been observed for the MsNork, the MtDmi2, and the LjSymRK mutant eguminous plants can engage into a symbiotic interaction lines. When care is taken not to disturb root hairs during Lwith rhizobia and form new root organs, the nodules, in which experimental manipulations, they curl upon application of rhi- the bacteria reside and fix atmospheric dinitrogen. Rhizobia zobia, but the curling is arrested when the root hair tip touches belong to diverse phylogenetic taxa but have in common the its own shank. Hence SymRK and its relatives are not needed for capacity to induce nodules on the appropriate legume host. The the curling process itself, although they do remain necessary for nodulation process is initiated by a complex signal exchange downstream, NF-dependent gene expression (18). We have investigated the role of SrSymRK, the unique between both partners. The principal signal molecules, the ͞ bacterial nodulation factors (NFs), are lipochitooligosaccharides Sesbania rostrata ortholog of MsNork LjSymRK in the estab- decorated with specific chemical groups at both the reducing and lishment of lateral root base (LRB) nodules. The tropical legume nonreducing end (1). Recognition of compatible NFs triggers S. rostrata is adapted to nodulate in temporarily flooded habitats developmental and cellular host responses, such as rapid ion and has versatile nodulation features. Under well-aerated con- fluxes, membrane depolarization, calcium oscillations, cytoskel- ditions, nodules form in the zone of developing root hairs via etal reorganization, root hair deformations and curling, gene RHC invasion of the microsymbiont Azorhizobium caulinodans expression, and cell division (2, 3). (19). However, on hydroponic roots, N2-fixing nodules develop Rhizobial invasion usually takes place via root hairs. Upon NF at LRBs (19). Azorhizobia invade the cortex intercellularly via perception, developing root hairs deform and eventually curl (4). cracks, resulting from lateral root protrusion, thereby circum- The bacteria are entrapped in this curl and a microcolony is venting the epidermis (20). Cortical infection pockets (IPs) are formed by NF-dependent local cell death induction and subse- formed. Local cell wall hydrolysis and invagination of the plasma quent colonization of bacteria. Presumably, IPs function as membrane lead to the formation of a tubular structure: the signaling centers, similar to rhizobial colonies within 3D root infection thread (IT) that proceeds through the root hair and hair curls (19). From IPs, ITs guide bacteria toward the target underlying cell layers to guide the bacteria toward a nodule cells for symbiotic uptake. A very comparable process takes primordium, which develops in the cortex (4). An elaborate IT place at the bases of adventitious rootlets that are located on the network spreads into the nodule primordium to provide bacteria stem of S. rostrata and that can develop into ‘‘stem’’ nodules upon to plant cells for endosymbiotic release. Uptake is initiated by inoculation. Because LRB nodulation with intercellular invasion local IT wall hydrolysis; unwalled infection droplets are formed from which bacteria are pinched off, thus creating symbiosomes (5). Symbiosomes contain one or a few bacteria, now called Abbreviations: dpi, days postinoculation; IP, infection pocket; IT, infection thread; NF, bacteroids, surrounded by a plant-derived membrane, the perib- nodulation factor; LRB, lateral root base; LRR, leucine-rich repeat; RHC, root hair curling; acteroid or symbiosome membrane (6). LysM, lysin motif; RNAi, RNA interference. Considerable progress has been made in analyzing the plant Data deposition: The sequence reported in this paper has been deposited in the GenBank mechanisms that regulate initiation and development of nodules database (accession no. AY751547). and control of bacterial invasion. Several candidate NF receptors *W.C. and S.G. contributed equally to this work. † have been identified, which are all receptor-like kinases with To whom correspondence should be addressed. E-mail: [email protected]. PLANT BIOLOGY extracellular lysin motif (LysM) domains (7–9). Bacterial LysM © 2005 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0504250102 PNAS ͉ July 19, 2005 ͉ vol. 102 ͉ no. 29 ͉ 10369–10374 Downloaded by guest on September 29, 2021 Fig. 1. SrSymRK, the SymRK ortholog of S. rostrata.(A) Sequence of the SrSymRK protein and orthologs. SrSymRK shows a 90% and 86% similarity to L. japonicus LjSymRK and M. truncatula MtDMI2, respectively. Conserved amino acids are highlighted. (B) Southern analysis with the extracellular domain of SrSymRK as a probe. strictly depends on NFs (21), it is an excellent tool to analyze the GAAGTGA-3Ј) and SrNORKrtR2 (5Ј-CTTCGCTCATGTGT- requirement for and consequences of NF-linked perception- TGGTTGC-3Ј) primers. transduction systems in cell layers, which are deeper than the epidermis. Here, we demonstrate that RNA interference Transgenic Roots. To produce the knockout constructs (RNAi)-mediated knockdown of SrSymRK inhibits release of (pK7GWIWG27F2-SymRKKO1 and pK7GWIWG27F2-Sym- bacteria from infection droplets into the plant cytoplasm. RKKO2), two nonoverlapping regions of the LRR domain were recombined in the pK7GWIWG27F2 binary GATEWAY vec- Materials and Methods tors (Invitrogen) (27). For the pK7GWIWG27F2-SymRKKO1 Plant and Bacterial Material. S. rostrata Brem and A. caulinodans and pK7GWIWG27F2-SymRKKO2 constructs, the primers Ј ORS571(pRG960SD-32) were grown as described (22). SrSymRKRTF1attB1 (5 -GGGGACAAGTTTGTACAAA- AAAGCAGGCTCCAACCAAACAGACGTGGAAGTGA- Ј Ј Southern Analysis. DNA gel blot analysis was performed as 3 ) and SrSymRKR13attB2 (5 -GGGACCACTTTGTACA- AGAAAGCTGGGTCACTGGAAGGAATTGGTCCT-3Ј); described (23). Labeled probes were generated from the extra- Ј Ј and SrSymRKF16attB1 (5 -GGGGACAAGTTTGTAC- cellular domain with SrNORKRTF1 (5 -CCAAACAGACGT- Ј Ј Ј AAAAAAGCAGGCTTGAGCCACAACAGT-3 ) and GGAAGTGA-3 ) and SrNORKRTR2 (5 -CTTCGCTCATGT- Ј Ј SrSymRKRTR2attB2 (5 -GGGGACCACTTTGTACAAGA- GTTGGTTGC-3 ). AAGCTGGGTCTTCGCTCATGTGTTGGTTGC-3Ј) were 5 used, respectively. S. rostrata embryonic axes were transformed Identification of the Full-Length SrSymRK Sequence. Plaques (10 )of as described (28). a ␭-fix II S. rostrata genomic library were screened with a probe corresponding to the extracellular and kinase domains of M. Light Microscopy and Transmission EM. Staining with ␤-glucuroni- truncatula DMI2 (23). The full-length cDNA sequence was dase was as described (21). For semithin sections, the tissues Ј Ј obtained by 5 and 3 RACE (Smart RACE cDNA
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