Genetic supressors of Lotus japonicus har1-1 hypernodulation show altered interactions with Glomus intraradices
Jeremy Murray A , Ryan Geil B , Cameron Wagg B , Bogumil Karas A , Krzysztof Szczyglowski A C and R. Larry Peterson BA Agriculture and Agri-Food Canada, Southern Crop Protection and Food Research Centre, London, Ontario N5V 4T3, Canada.
B Department of Integrative Biology, University of Guelph, Guelph, Ontario N1G 2W1, Canada.
C Corresponding author. Email: szczyglowskik@agr.gc.ca
D This paper originates from a presentation at the Third International Conference on Legume Genomics and Genetics, Brisbane, Queensland, Australia, April 2006.
Functional Plant Biology 33(8) 749-755 https://doi.org/10.1071/FP06083
Submitted: 10 April 2006 Accepted: 19 May 2006 Published: 2 August 2006
Abstract
Mutant lines of Lotus japonicus (Regel) Larsen that show defects in nodulation as well as in mycorrhiza formation are valuable resources for studying the events required for the establishment of functional symbioses. In this study, 11 mutant lines derived from a screen for genetic suppressors of har1-1 hypernodulation were assessed quantitatively for their ability to form arbuscular mycorrhizal (AM) symbiosis. The presence of extraradical mycelia, appressoria, intraradical hyphae, arbuscules and vesicles were scored. Roots of the har1-1 parental line were heavily colonised by six weeks after inoculation with the AM fungus Glomus intraradices showing the typical Arum-type colonisation pattern. Five mutants lacked internal root colonisation with blocks either at the surface of epidermal cells or at the outer tangential wall of cortical cells. These AM– lines showed some differences in relation to the amount of extraradical hyphae, the number of appressoria, and the degree of abnormal appressorium morphology. Four mutants had internal root colonisation but at a lower level than the parental line. Two mutants showed no difference from the parental line. Results of this study provide additional genetic resources for studying the mechanism of root colonisation by AM fungi.
Keywords: AM, CASTOR, CCaMK, epidermis, Glomus intraradices, LjPRH1, Lotus japonicus, mutants, NFR5, POLLUX, root hair, SYM24, SYM7.
Acknowledgments
This research was supported by Agriculture and Agri-Food Canada Crop Genomics Initiative and Natural Sciences and Engineering Research Council of Canada grant award no. 3277A01 to KS and a Natural Sciences and Engineering Research Council of Canada Discovery Grant to RLP. We thank Lewis Melville for help with the figures.
Akiyama K,
Matsuzaki K-I, Hayashi H
(2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824–827.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Albrecht C,
Geurts R,
Lapeyrie F, Bisseling T
(1998) Endomycorrhizae and rhizobial Nod factors both require SYM8 to induce the expression of the early nodulin genes PsENOD5 and PsENOD12A. The Plant Journal 15, 605–614.
| Crossref | GoogleScholarGoogle Scholar |
Bonfante P,
Genre A,
Faccio A,
Martini I,
Schauser L,
Stougaard J,
Webb J, Parniske M
(2000) The Lotus japonicus LjSym4 gene is required for the successful symbiotic infection of root epidermal cells. Molecular Plant–Microbe Interactions 13, 1109–1120.
| PubMed |
Bradbury SM,
Peterson RL, Bowley SR
(1991) Interactions between three alfalfa nodulation genotypes and two Glomus species. New Phytologist 119, 115–120.
| Crossref | GoogleScholarGoogle Scholar |
Bradbury SM,
Peterson RL, Bowley SR
(1993) Further evidence for a correlation between nodulation genotypes in alfalfa (Medicago sativa L.) and mycorrhiza formation. New Phytologist 124, 665–673.
| Crossref | GoogleScholarGoogle Scholar |
Buee M,
Rossignol M,
Jauneau A,
Ranjeva R, Bécard G
(2000) The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Molecular Plant–Microbe Interactions 13, 693–698.
| PubMed |
Calantzis C,
Morandi D,
Arnould C, Gianinazzi-Pearson V
(2001) Cellular interactions between G. mosseae and a myc– dmi2 mutant in Medicago truncatula. Symbiosis 30, 97–108.
Demchenko K,
Winzer T,
Stougaard J,
Parniske M, Pawlowski K
(2004) Distinct roles of Lotus japonicus SYMRK and SYM15 in root colonization and arbuscule formation. New Phytologist 163, 381–392.
| Crossref | GoogleScholarGoogle Scholar |
Genre A, Bonfante P
(2002) Epidermal cells of a symbiosis-defective mutant of Lotus japonicus show altered cytoskeleton organization in the presence of a mycorrhizal fungus. Protoplasma 219, 43–50.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Genre A, Bonfante P
(2005) Building a mycorrhizal cell: how to reach compatibility between plants and arbuscular mycorrhizal fungi. Journal of Plant Interactions 1, 3–13.
| Crossref | GoogleScholarGoogle Scholar |
Hirsch AM, Kapulnik Y
(1998) Signal transduction pathways in mycorrhizal associations: comparisons with the Rhizobium–legume symbiosis. Fungal Genetics and Biology 23, 205–212.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jacobi LM,
Zubkova LA,
Barmicheva EM,
Tsyganov VE,
Borisov AY, Tikhonovich IA
(2003) Effect of mutations in the pea genes Sym33 and Sym40 II. Dynamics of arbuscule development and turnover. Mycorrhiza 13, 9–16.
| PubMed |
Karas B,
Murray J,
Gorzelak M,
Smith A,
Sato S,
Tabata S, Szczyglowski K
(2005) Invasion of Lotus japonicus root hairless 1 by Mezorhizobium loti involves the Nod factor dependent induction of root hairs. Plant Physiology 137, 1331–1344.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kistner C,
Winzer T,
Pitzschke A,
Mulder L, Sato S , et al.
(2005) Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. The Plant Cell 17, 2217–2229.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Krusell L,
Madsen LH,
Sato S,
Aubert G, Genua A , et al.
(2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420, 422–426.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Marsh JF, Schultze M
(2001) Analysis of arbuscular mycorrhizas using symbiosis-defective plant mutants. New Phytologist 150, 525–532.
| Crossref | GoogleScholarGoogle Scholar |
McGonigle TP,
Miller MH,
Evans DG,
Fairchild GL, Swan JA
(1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular fungi. New Phytologist 115, 495–501.
| Crossref | GoogleScholarGoogle Scholar |
Morandi D,
Sagan M,
Prado-Vivant E, Duc G
(2000) Influence of genes determining supernodulation on root colonization by the mycorrhizal fungus Glomus mosseae in Pisum sativum and Medicago truncatula mutants. Mycorrhiza 10, 37–42.
| Crossref | GoogleScholarGoogle Scholar |
Murray J,
Karas B,
Ross L,
Brachmann A,
Wagg C,
Geil R,
Perry J,
Nowakowski K,
MacGillivary M,
Held M,
Stougaard J,
Peterson L,
Parniske M, Szczyglowski K
(2006) Genetic suppressors of the Lotus japonicus har1-1 hypernodulation phenotype. Molecular Plant–Microbe Interactions ,
| PubMed |
Novero M,
Faccio A,
Genre A,
Stougaard J,
Webb KJ,
Mulder L,
Parniske M, Bonfante P
(2002) Dual requirement of the LjSym4 gene for the mycorrhizal development in epidermal cells and cortical cells of Lotus japonicus roots. New Phytologist 154, 741–749.
| Crossref | GoogleScholarGoogle Scholar |
Parniske M
(2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Current Opinion in Plant Biology 7, 414–421.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Podila GK
(2002) Signaling in mycorrhizal symbioses — elegant mutants lead the way. New Phytologist 154, 541–545.
| Crossref | GoogleScholarGoogle Scholar |
Schauser L,
Handberg K,
Sandal N,
Stiller J,
Thykjær T,
Pajuelo E,
Nielsen A, Stougaard J
(1998) Symbiotic mutants deficient in nodule establishment identified after T-DNA transformation of Lotus japonicus. Molecular and General Genetics 259, 414–423.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Senoo K,
Solaiman MZ,
Kawaguchi M,
Imaizumi-Anraku H,
Akao S,
Tanaka A, Obata H
(2000) Isolation of two different phenotypes of mycorrhizal mutants in the model legume plant Lotus japonicus after EMS-treatment. Plant and Cell Physiology 41, 726–732.
| PubMed |
Shrihari PC,
Sakamoto K,
Inubushi K, Akao S
(2000) Interaction between supernodulating or non-nodulating mutants of soybean and two arbuscular mycorrhizal fungi. Mycorrhiza 10, 101–106.
| Crossref | GoogleScholarGoogle Scholar |
Solaiman MZ,
Senoo K,
Kawaguchi M,
Imaizumi-Anraku H,
Akao S,
Tanaka A, Obata H
(2000) Characterization of mycorrhizas formed by Glomus sp. on roots of hypernodulating mutants of Lotus japonicus. Journal of Plant Research 113, 443–448.
| Crossref | GoogleScholarGoogle Scholar |
Szczyglowski K,
Shaw RS,
Wopereis J,
Copeland S,
Hamburger D,
Kasiborski B,
Dazzo FB, de Bruijn FJ
(1998) Nodule organogenesis and symbiotic mutants of the model legume Lotus japonicus. Molecular Plant–Microbe Interactions 11, 684–697.
Vierheilig H,
Coughlan AP,
Wyss U, Piché Y
(1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Applied and Environmental Microbiology 64, 5004–5007.
| PubMed |
Wegel E,
Schauser L,
Sandal N,
Stougaard J, Parniske M
(1998) Mycorrhiza mutants of Lotus japonicus define genetically independent steps during symbiotic infection. Molecular Plant–Microbe Interactions 11, 933–936.
Wopereis J,
Pajuelo E,
Dazzo FB,
Jiang Q,
Gresshoff PM,
de Bruijn FJ,
Stougaard J, Szczyglowski K
(2000) Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. The Plant Journal 23, 97–114.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
