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PMID: 20409002 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts.

The Plant journal : for cell and molecular biology ·Vol. 63 ·No. 1 ·2010-07-01 ·Pages 141-54

Hayashi T, Banba M, Shimoda Y, Kouchi H, Hayashi M, Imaizumi-Anraku H

Abstract

In legumes, Ca(2+)/calmodulin-dependent protein kinase (CCaMK) is a component of the common symbiosis genes that are required for both root nodule (RN) and arbuscular mycorrhiza (AM) symbioses and is thought to be a decoder of Ca(2+) spiking, one of the earliest cellular responses to microbial signals. A gain-of-function mutation of CCaMK has been shown to induce spontaneous nodulation without rhizobia, but the significance of CCaMK activation in bacterial and/or fungal infection processes is not fully understood. Here we show that a gain-of-function CCaMK(T265D) suppresses loss-of-function mutations of common symbiosis genes required for the generation of Ca(2+) spiking, not only for nodule organogenesis but also for successful infection of rhizobia and AM fungi, demonstrating that the common symbiosis genes upstream of Ca(2+) spiking are required solely to activate CCaMK. In RN symbiosis, however, CCaMK(T265D) induced nodule organogenesis, but not rhizobial infection, on Nod factor receptor (NFRs) mutants. We propose a model of symbiotic signaling in host legume plants, in which CCaMK plays a key role in the coordinated induction of infection thread formation and nodule organogenesis.

MeSH Terms
Bacteria/growth & development Calcium/metabolism Calcium-Calmodulin-Dependent Protein Kinases/genetics,metabolism Gene Expression Regulation, Plant Genetic Complementation Test Lotus/enzymology,genetics,microbiology Mutation Mycorrhizae/growth & development Plant Proteins/genetics,metabolism Plant Root Nodulation/genetics Symbiosis/genetics Transformation, Genetic
Chemicals
Plant Proteins Calcium-Calmodulin-Dependent Protein Kinases Calcium
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Hayashi Teruyuki
National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan.
Banba Mari
Shimoda Yoshikazu
Kouchi Hiroshi
Hayashi Makoto
Imaizumi-Anraku Haruko
References (71)
71 references, click to expand
  1. A plant regulator controlling development of symbiotic root nodules.
    Nature. 1999 Nov 11;402(6758):191-5 PMID: 10647012
  2. Cytokinin: secret agent of symbiosis.
    Trends Plant Sci. 2008 Mar;13(3):115-20 PMID: 18296104
  3. Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development.
    Nature. 2006 Jun 29;441(7097):1153-6 PMID: 16810257
  4. Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase.
    Plant Physiol. 2007 May;144(1):324-35 PMID: 17369436
  5. Nod factor elicits two separable calcium responses in Medicago truncatula root hair cells.
    Plant Physiol. 2003 Mar;131(3):976-84 PMID: 12644650
  6. Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DMI2.
    Proc Natl Acad Sci U S A. 2005 Jul 19;102(29):10375-80 PMID: 16006515
  7. A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis.
    Science. 2007 Jan 5;315(5808):104-7 PMID: 17110537
  8. Responses of a model legume Lotus japonicus to lipochitin oligosaccharide nodulation factors purified from Mesorhizobium loti JRL501.
    Mol Plant Microbe Interact. 2001 Jul;14(7):848-56 PMID: 11437258
  9. Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes.
    Science. 2004 Feb 27;303(5662):1364-7 PMID: 14963334
  10. De novo organ formation from differentiated cells: root nodule organogenesis.
    Sci Signal. 2008 Dec 09;1(49):re11 PMID: 19066400
  11. A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula.
    Plant Physiol. 2003 Mar;131(3):952-62 PMID: 12644648
  12. 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. 2006 Dec 31;13(6):255-65 PMID: 17244637
  13. Structural identification of the lipo-chitin oligosaccharide nodulation signals of Rhizobium loti.
    Mol Microbiol. 1995 Feb;15(4):627-38 PMID: 7783635
  14. Nod factor signaling genes and their function in the early stages of Rhizobium infection.
    Curr Opin Plant Biol. 2005 Aug;8(4):346-52 PMID: 15955723
  15. Multifunctional Ca2+/calmodulin-dependent protein kinase made Ca2+ independent for functional studies.
    Biochemistry. 1990 Feb 20;29(7):1679-84 PMID: 2158811
  16. Divergence of evolutionary ways among common sym genes: CASTOR and CCaMK show functional conservation between two symbiosis systems and constitute the root of a common signaling pathway.
    Plant Cell Physiol. 2008 Nov;49(11):1659-71 PMID: 18852152
  17. 3-hydroxy-3-methylglutaryl coenzyme a reductase 1 interacts with NORK and is crucial for nodulation in Medicago truncatula.
    Plant Cell. 2007 Dec;19(12):3974-89 PMID: 18156218
  18. SrSymRK, a plant receptor essential for symbiosome formation.
    Proc Natl Acad Sci U S A. 2005 Jul 19;102(29):10369-74 PMID: 16006516
  19. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals.
    Cell. 1996 May 31;85(5):673-81 PMID: 8646776
  20. A plant receptor-like kinase required for both bacterial and fungal symbiosis.
    Nature. 2002 Jun 27;417(6892):959-62 PMID: 12087405
  21. Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis.
    Plant Cell. 2005 Aug;17(8):2217-29 PMID: 15980262
  22. Tracing nonlegume orthologs of legume genes required for nodulation and arbuscular mycorrhizal symbioses.
    Genetics. 2006 Apr;172(4):2491-9 PMID: 16452143
  23. LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range.
    EMBO J. 2007 Sep 5;26(17):3923-35 PMID: 17690687
  24. Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses.
    Plant Cell. 1994 Oct;6(10):1357-74 PMID: 7994171
  25. Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots.
    Nature. 2005 Feb 3;433(7025):527-31 PMID: 15616514
  26. Antiquity and function of CASTOR and POLLUX, the twin ion channel-encoding genes key to the evolution of root symbioses in plants.
    Plant Physiol. 2009 Jan;149(1):306-17 PMID: 18978069
  27. Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway.
    Plant Cell. 2008 Nov;20(11):2989-3005 PMID: 19033527
  28. A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis.
    Science. 2007 Jan 5;315(5808):101-4 PMID: 17110535
  29. Acetylation of a fucosyl residue at the reducing end of Mesorhizobium loti nod factors is not essential for nodulation of Lotus japonicus.
    Plant Cell Physiol. 2005 Jun;46(6):1016-20 PMID: 15805124
  30. Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria.
    PLoS Biol. 2008 Mar 4;6(3):e68 PMID: 18318603
  31. Inhibition of G2/M progression in Schizosaccharomyces pombe by a mutant calmodulin kinase II with constitutive activity.
    Mol Biol Cell. 1994 Jul;5(7):785-95 PMID: 7812047
  32. Fungal symbiosis in rice requires an ortholog of a legume common symbiosis gene encoding a Ca2+/calmodulin-dependent protein kinase.
    Plant Physiol. 2007 Dec;145(4):1619-28 PMID: 17965173
  33. Ca2+-dependent protein kinases and stress signal transduction in plants.
    Science. 1996 Dec 13;274(5294):1900-2 PMID: 8943201
  34. The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus.
    Nat Commun. 2010 Apr 12;1:10 PMID: 20975672
  35. New nodulation mutants responsible for infection thread development in Lotus japonicus.
    Mol Plant Microbe Interact. 2006 Jul;19(7):801-10 PMID: 16838792
  36. Analysis of Nod-factor-induced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus.
    Mol Plant Microbe Interact. 2006 Aug;19(8):914-23 PMID: 16903357
  37. Plant science. Nodules and hormones.
    Science. 2007 Jan 5;315(5808):52-3 PMID: 17204633
  38. NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus.
    Plant Cell. 2007 Feb;19(2):610-24 PMID: 17307929
  39. Evolution and regulation of the Lotus japonicus LysM receptor gene family.
    Mol Plant Microbe Interact. 2010 Apr;23(4):510-21 PMID: 20192837
  40. CYCLOPS, a mediator of symbiotic intracellular accommodation.
    Proc Natl Acad Sci U S A. 2008 Dec 23;105(51):20540-5 PMID: 19074278
  41. A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses.
    Science. 2004 Feb 27;303(5662):1361-4 PMID: 14963335
  42. Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition.
    Nature. 2006 Jun 29;441(7097):1149-52 PMID: 16810256
  43. Structure-function of the multifunctional Ca2+/calmodulin-dependent protein kinase II.
    Biochem J. 2002 Jun 15;364(Pt 3):593-611 PMID: 11931644
  44. The Medicago truncatula lysin [corrected] motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes.
    Plant Physiol. 2006 Sep;142(1):265-79 PMID: 16844829
  45. Cytokinins play opposite roles in lateral root formation, and nematode and Rhizobial symbioses.
    Plant J. 2004 Apr;38(2):203-14 PMID: 15078325
  46. Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators.
    Science. 2005 Jun 17;308(5729):1786-9 PMID: 15961668
  47. CERBERUS, a novel U-box protein containing WD-40 repeats, is required for formation of the infection thread and nodule development in the legume-Rhizobium symbiosis.
    Plant J. 2009 Oct;60(1):168-80 PMID: 19508425
  48. Arbuscular mycorrhiza: the mother of plant root endosymbioses.
    Nat Rev Microbiol. 2008 Oct;6(10):763-75 PMID: 18794914
  49. crinkle, a novel symbiotic mutant that affects the infection thread growth and alters the root hair, trichome, and seed development in Lotus japonicus.
    Plant Physiol. 2003 Mar;131(3):1054-63 PMID: 12644658
  50. Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes.
    Proc Natl Acad Sci U S A. 2008 Jul 15;105(28):9823-8 PMID: 18606999
  51. Medicago LYK3, an entry receptor in rhizobial nodulation factor signaling.
    Plant Physiol. 2007 Sep;145(1):183-91 PMID: 17586690
  52. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal.
    Nature. 1990 Apr 19;344(6268):781-4 PMID: 2330031
  53. NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription.
    Science. 2005 Jun 17;308(5729):1789-91 PMID: 15961669
  54. A receptor kinase gene regulating symbiotic nodule development.
    Nature. 2002 Jun 27;417(6892):962-6 PMID: 12087406
  55. OsIPD3, an ortholog of the Medicago truncatula DMI3 interacting protein IPD3, is required for mycorrhizal symbiosis in rice.
    New Phytol. 2008;180(2):311-315 PMID: 18761634
  56. Coordinating nodule morphogenesis with rhizobial infection in legumes.
    Annu Rev Plant Biol. 2008;59:519-46 PMID: 18444906
  57. Genetic suppressors of the Lotus japonicus har1-1 hypernodulation phenotype.
    Mol Plant Microbe Interact. 2006 Oct;19(10):1082-91 PMID: 17022172
  58. Lotus japonicus nodulation requires two GRAS domain regulators, one of which is functionally conserved in a non-legume.
    Plant Physiol. 2006 Dec;142(4):1739-50 PMID: 17071642
  59. Gibberellin controls the nodulation signaling pathway in Lotus japonicus.
    Plant J. 2009 Apr;58(2):183-94 PMID: 19121107
  60. The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation.
    Plant J. 2003 May;34(4):495-506 PMID: 12753588
  61. Knockdown of an arbuscular mycorrhiza-inducible phosphate transporter gene of Lotus japonicus suppresses mutualistic symbiosis.
    Plant Cell Physiol. 2006 Jul;47(7):807-17 PMID: 16774930
  62. The HCL gene of Medicago truncatula controls Rhizobium-induced root hair curling.
    Development. 2001 May;128(9):1507-18 PMID: 11290290
  63. Expression of the Medicago truncatula DM12 gene suggests roles of the symbiotic nodulation receptor kinase in nodules and during early nodule development.
    Mol Plant Microbe Interact. 2005 Aug;18(8):869-76 PMID: 16134899
  64. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals.
    Nature. 2003 Oct 9;425(6958):637-40 PMID: 14534591
  65. Evolution of root endosymbiosis with bacteria: How novel are nodules?
    Trends Plant Sci. 2009 Feb;14(2):77-86 PMID: 19167260
  66. A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis.
    Proc Natl Acad Sci U S A. 2006 Jan 10;103(2):359-64 PMID: 16407163
  67. A novel ARID DNA-binding protein interacts with SymRK and is expressed during early nodule development in Lotus japonicus.
    Plant Physiol. 2008 Sep;148(1):337-47 PMID: 18633121
  68. The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti.
    Plant Cell. 2006 Oct;18(10):2680-93 PMID: 17028204
  69. SYMRK, an enigmatic receptor guarding and guiding microbial endosymbioses with plant roots.
    Proc Natl Acad Sci U S A. 2008 Mar 25;105(12):4537-8 PMID: 18349141
  70. Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula.
    Proc Natl Acad Sci U S A. 2000 Nov 21;97(24):13407-12 PMID: 11078514
  71. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases.
    Nature. 2003 Oct 9;425(6958):585-92 PMID: 14534578
Article Info
Journal
The Plant journal : for cell and molecular biology
Abbr.
Plant J
ISSN
1365-313X
Published
2010-07-01
Epub
2010-00-16
Pages
141-54
Language
English
Region
England
NLM ID
9207397
PMCID
PMC2916219
Subset
IM
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