The Molecular Network Governing Nodule Organogenesis and Infection in the Model Legume Lotus Japonicus

Overview

Journal Nat Commun

Specialty Biology

Date 2010 Oct 27

PMID 20975672

Citations 165

Authors

Lene H Madsen

Leila Tirichine

Anna Jurkiewicz

John T Sullivan

Anne B Heckmann

Anita S Bek

Clive W Ronson

Euan K James

Jens Stougaard

Affiliations

Soon will be listed here.

Abstract

Bacterial infection of interior tissues of legume root nodules is controlled at the epidermal cell layer and is closely coordinated with progressing organ development. Using spontaneous nodulating Lotus japonicus plant mutants to uncouple nodule organogenesis from infection, we have determined the role of 16 genes in these two developmental processes. We show that host-encoded mechanisms control three alternative entry processes operating in the epidermis, the root cortex and at the single cell level. Single cell infection did not involve the formation of trans-cellular infection threads and was independent of host Nod-factor receptors and bacterial Nod-factor signals. In contrast, Nod-factor perception was required for epidermal root hair infection threads, whereas primary signal transduction genes preceding the secondary Ca2+ oscillations have an indirect role. We provide support for the origin of rhizobial infection through direct intercellular epidermal invasion and subsequent evolution of crack entry and root hair invasions observed in most extant legumes.

Citing Articles

Nitrogen and Nod factor signaling determine Lotus japonicus root exudate composition and bacterial assembly.

Tao K, Jensen I, Zhang S, Villa-Rodriguez E, Blahovska Z, Salomonsen C Nat Commun. 2024; 15(1):3436.

PMID: 38653767 PMC: 11039659. DOI: 10.1038/s41467-024-47752-0.

A Novel Rhizobium sp. Chiba-1 Strain Exhibits a Host Range for Nodule Symbiosis in Lotus Species.

Chiba Y, Sasaki M, Masuda S, Shibata A, Shirasu K, Kawaharada Y Microbes Environ. 2023; 38(4).

PMID: 38044128 PMC: 10728632. DOI: 10.1264/jsme2.ME23056.

Single-cell analysis identifies genes facilitating rhizobium infection in Lotus japonicus.

Frank M, Fechete L, Tedeschi F, Nadzieja M, Norgaard M, Montiel J Nat Commun. 2023; 14(1):7171.

PMID: 37935666 PMC: 10630511. DOI: 10.1038/s41467-023-42911-1.

Both incompatible and compatible rhizobia inhabit the intercellular spaces of leguminous root nodules.

Hata S, Tsuda R, Kojima S, Tanaka A, Kouchi H Plant Signal Behav. 2023; 18(1):2245995.

PMID: 37573516 PMC: 10424618. DOI: 10.1080/15592324.2023.2245995.

G-type receptor-like kinase AsNIP43 interacts with rhizobia effector nodulation outer protein P and is required for symbiosis.

Liu Y, Lin Y, Wei F, Lv Y, Xie F, Chen D Plant Physiol. 2023; 193(2):1527-1546.

PMID: 37432453 PMC: 10517198. DOI: 10.1093/plphys/kiad318.

References

Ane J, Kiss G, Riely B, Penmetsa R, Oldroyd G, Ayax C . Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science. 2004; 303(5662):1364-7. DOI: 10.1126/science.1092986. View

Schauser L, Roussis A, Stiller J, Stougaard J . A plant regulator controlling development of symbiotic root nodules. Nature. 2000; 402(6758):191-5. DOI: 10.1038/46058. View

Radutoiu S, Madsen L, Madsen E, Jurkiewicz A, Fukai E, Quistgaard E . LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J. 2007; 26(17):3923-35. PMC: 1994126. DOI: 10.1038/sj.emboj.7601826. View

Murray J, Karas B, Sato S, Tabata S, Amyot L, Szczyglowski K . A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science. 2006; 315(5808):101-4. DOI: 10.1126/science.1132514. View

Middleton P, Jakab J, Penmetsa R, Starker C, Doll J, Kalo P . An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction. Plant Cell. 2007; 19(4):1221-34. PMC: 1913751. DOI: 10.1105/tpc.106.048264. View

Tirichine L, Imaizumi-Anraku H, Yoshida S, Murakami Y, Madsen L, Miwa H . Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature. 2006; 441(7097):1153-6. DOI: 10.1038/nature04862. View

Esseling J, Lhuissier F, Emons A . A nonsymbiotic root hair tip growth phenotype in NORK-mutated legumes: implications for nodulation factor-induced signaling and formation of a multifaceted root hair pocket for bacteria. Plant Cell. 2004; 16(4):933-44. PMC: 412867. DOI: 10.1105/tpc.019653. View

Tirichine L, Sandal N, Madsen L, Radutoiu S, Albrektsen A, Sato S . A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science. 2006; 315(5808):104-7. DOI: 10.1126/science.1132397. View

Murakami Y, Miwa H, Imaizumi-Anraku H, Kouchi H, Downie J, Kawaguchi M . Positional cloning identifies Lotus japonicus NSP2, a putative transcription factor of the GRAS family, required for NIN and ENOD40 gene expression in nodule initiation. DNA Res. 2007; 13(6):255-65. DOI: 10.1093/dnares/dsl017. View

10.

Van den Berg J, Thomas-Oates J, Glushka J, Lugtenberg B, Spaink H . Structural identification of the lipo-chitin oligosaccharide nodulation signals of Rhizobium loti. Mol Microbiol. 1995; 15(4):627-38. DOI: 10.1111/j.1365-2958.1995.tb02372.x. View

11.

Mitra R, Gleason C, Edwards A, Hadfield J, Downie J, Oldroyd G . A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: Gene identification by transcript-based cloning. Proc Natl Acad Sci U S A. 2004; 101(13):4701-5. PMC: 384810. DOI: 10.1073/pnas.0400595101. View

12.

Mitra R, Shaw S, Long S . Six nonnodulating plant mutants defective for Nod factor-induced transcriptional changes associated with the legume-rhizobia symbiosis. Proc Natl Acad Sci U S A. 2004; 101(27):10217-22. PMC: 454190. DOI: 10.1073/pnas.0402186101. View

13.

Capoen W, Goormachtig S, De Rycke R, Schroeyers K, Holsters M . SrSymRK, a plant receptor essential for symbiosome formation. Proc Natl Acad Sci U S A. 2005; 102(29):10369-74. PMC: 1177396. DOI: 10.1073/pnas.0504250102. View

14.

Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T . A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature. 2002; 417(6892):959-62. DOI: 10.1038/nature00841. View

15.

Gage D . Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev. 2004; 68(2):280-300. PMC: 419923. DOI: 10.1128/MMBR.68.2.280-300.2004. View

16.

Capoen W, Den Herder J, Sun J, Verplancke C, De Keyser A, De Rycke R . Calcium spiking patterns and the role of the calcium/calmodulin-dependent kinase CCaMK in lateral root base nodulation of Sesbania rostrata. Plant Cell. 2009; 21(5):1526-40. PMC: 2700542. DOI: 10.1105/tpc.109.066233. View

17.

Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H, Umehara Y . Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature. 2004; 433(7025):527-31. DOI: 10.1038/nature03237. View

18.

Hogslund N, Radutoiu S, Krusell L, Voroshilova V, Hannah M, Goffard N . Dissection of symbiosis and organ development by integrated transcriptome analysis of lotus japonicus mutant and wild-type plants. PLoS One. 2009; 4(8):e6556. PMC: 2717213. DOI: 10.1371/journal.pone.0006556. View

19.

Asamizu E, Shimoda Y, Kouchi H, Tabata S, Sato S . A positive regulatory role for LjERF1 in the nodulation process is revealed by systematic analysis of nodule-associated transcription factors of Lotus japonicus. Plant Physiol. 2008; 147(4):2030-40. PMC: 2492631. DOI: 10.1104/pp.108.118141. View

20.

Miwa H, Sun J, Oldroyd G, Downie J . Analysis of Nod-factor-induced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus. Mol Plant Microbe Interact. 2006; 19(8):914-23. DOI: 10.1094/MPMI-19-0914. View