The rmc locus does not affect plant interactions or defence-related gene expression when tomato (Solanum lycopersicum) is infected with the root fungal parasite, Rhizoctonia
Ling-Ling Gao A B C , F. Andrew Smith A and Sally E. Smith AA Soil and Land Systems and the Centre for Soil–Plant Interactions, School of Earth and Environmental Sciences, The University of Adelaide, Adelaide, SA 5005, Australia.
B Current address: CSIRO Plant Industry, Private Bag 5, Wembley, WA 6913, Australia.
C Corresponding author. Email: lingling.gao@csiro.au
Functional Plant Biology 33(3) 289-296 https://doi.org/10.1071/FP05153
Submitted: 27 June 2005 Accepted: 7 November 2005 Published: 2 March 2006
Abstract
A tomato mutant with reduced mycorrhizal colonisation, rmc, confers resistance to almost all arbuscular mycorrhizal (AM) fungal species tested, although there is variation in colonisation of different root cell layers by different fungi and one species of AM fungus can colonise this mutant relatively normally. These variations indicate a high degree of specificity in relation to AM colonisation. We explored the possibility of specificity or otherwise in interactions between rmc and three non-AM root-infecting fungi, Rhizoctonia solani anastomosis groups (AG) 4 and AG8, and binucleate Rhizoctonia (BNR). There were no differences between the wild type tomato 76R and rmc in the speed or extent to which these fungi infected roots or caused disease. Infection by R. solani induced high levels of defence-related gene expression in both tomato genotypes relative to non-infected plants. In contrast, with BNR the expression of these genes was not induced or induced to a much lower extent than with R. solani. The expression of defence-related genes with these two non-AM fungi was very similar in the two plant genotypes. It was different from effects observed during colonisation by AM fungi, which enhanced expression of defence-related genes in rmc compared with the wild type tomato. The specificity and molecular mechanisms of rmc in control of AM colonisation are discussed.
Keywords: arbuscular mycorrhiza, mycorrhiza-defective mutant, symbiosis, root disease.
Acknowledgments
We thank Ms Debbie Miller for excellent technical support. Ling-Ling Gao thanks Dr Wolfgang Knogge and Dr Gabriele Delp for supervision during her PhD study. L.-L. Gao also acknowledges the receipt of an Adelaide International Postgraduate Research Scholarship. The work was supported by the Australian Research Council and a University of Adelaide Small Grant. We are grateful to Drs J. van Kan, Department of Phytopathology, Wageningen Agricultural University, Wageningen, The Netherlands and J. Robb, Department of Molecular Biology and Genetics, University of Guelph, Ontario, Canada, who made the cDNA clones available to us.
Barker SJ,
Stummer B,
Gao L,
Dispain I,
O’Connor PJ, Smith SE
(1998) A mutant in Lycopersicon esculentum Mill. with highly reduced VA mycorrhizal colonization: isolation and preliminary characterisation. The Plant Journal 15, 791–797.
| Crossref | GoogleScholarGoogle Scholar |
Cavagnaro TR,
Smith FA,
Lorimer MF,
Haskard KA,
Ayling SM, Smith SE
(2001) Quantitative development of Paris-type arbuscular mycorrhizas formed between Asphodelus fistulosus and Glomus coronatum. New Phytologist 149, 105–113.
| Crossref | GoogleScholarGoogle Scholar |
Colwell JD
(1963) The estimation of the phosphorus fertilizer requirements of wheat in southern New South Wales. Australian Journal of Experimental Agriculture and Animal Husbandry 3, 190–197.
| Crossref | GoogleScholarGoogle Scholar |
David-Schwartz R,
Badani H,
Smadar W,
Levy AA,
Galili G, Kapulnik Y
(2001) Identification of a novel genetically controlled step in mycorrhizal colonization: plant resistance to infection by fungal spores but not extra-radical hyphae. The Plant Journal 27, 561–569.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
David-Schwartz R,
Gadkar V,
Wininger S,
Bendov R,
Galili G,
Levy AA, Kapulnik Y
(2003) Isolation of a premycorrhizal infection (pmi2) mutant of tomato, resistant to arbuscular mycorrhizal fungal colonization. Molecular Plant–Microbe Interactions 16, 382–388.
| PubMed |
Duc G,
Trouvelot A,
Gianinazzi-Pearson V, Gianinazzi S
(1989) First report of non-mycorrhizal plant mutants (Myc-) obtained in pea (Pisum sativum L.) and fababean (Vicia faba L.). Plant Science 60, 215–222.
| Crossref | GoogleScholarGoogle Scholar |
Gao L-L,
Delp G, Smith SE
(2001) Colonization patterns in a mycorrhiza-defective mutant tomato vary with different arbuscular-mycorrhizal fungi. New Phytologist 151, 477–491.
| Crossref | GoogleScholarGoogle Scholar |
Gao L-L,
Knogge W,
Delp G,
Smith FA, Smith SE
(2004) Expression patterns of defense-related genes in different types of arbuscular mycorrhizal development in wild-type and mycorrhiza-defective mutant tomato. Molecular Plant–Microbe Interactions 17, 1103–1113.
| PubMed |
Gianinazzi-Pearson, V (1984). Host–fungus specificity, recognition and compatibility in mycorrhizae. In ‘Genes involved in microbe–plant interactions’. pp. 225–253. (Springer-Verlag: Wien)
Gianinazzi-Pearson V
(1996) Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis. The Plant Cell 8, 1871–1883.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Giovannetti M, Mosse B
(1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytologist 84, 489–500.
Helgason T,
Merryweather JW,
Denison J,
Wilson P,
Young JPW, Fitter AH
(2002) Selectivity and functional diversity in arbuscular mycorrhizas of co-occurring fungi and plants from a temperate deciduous woodland. Journal of Ecology 90, 371–384.
| Crossref | GoogleScholarGoogle Scholar |
Jabaji-Hare SH,
Chamberland H, Charest PM
(1999) Cell wall alterations in hypocotyls of bean seedlings protected from Rhizoctonia stem canker by a binucleate Rhizoctonia isolate. Mycological Research 103, 1035–1043.
| Crossref | GoogleScholarGoogle Scholar |
Kasiamdari RS,
Smith SE,
Scott ES, Smith FA
(2002a) Identification of binucleate Rhizoctonia as a contaminant of pot cultures of arbuscular mycorrhizal fungi and development of a PCR-based method of detection. Mycological Research 106, 1417–1426.
| Crossref | GoogleScholarGoogle Scholar |
Kasiamdari RS,
Smith SE,
Smith FA, Scott ES
(2002b) Influence of the mycorrhizal fungus, Glomus coronatum and soil phosphorus on infection and disease caused by binucleate Rhizoctonia and Rhizoctonia solani on mung bean (Vigna radiata). Plant and Soil 238, 235–244.
| Crossref | GoogleScholarGoogle Scholar |
Kunkel BN, Brooks DM
(2002) Cross talk between signaling pathways in pathogen defense. Current Opinion in Plant Biology 5, 325–331.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lee SW,
Nazar RN,
Powell DA, Robb J
(1992) Reduced PAL gene suppression in Verticillium-infected resistant tomatoes. Plant Molecular Biology 18, 345–352.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lewis DH
(1973) Concepts in fungal nutrition and the origin of biotrophy. Biological Reviews 48, 261–278.
Marsh JF, Schultze M
(2001) Analysis of arbuscular mycorrhizas using symbiosis-defective plant mutants. New Phytologist 150, 525–532.
| Crossref |
McDonald, HJ ,
and
Rovira, AD (1985). Development of an inoculation technique for Rhizoctonia solani and its application to screening cereal cultivars for resistance. In ‘Ecology and management of soil-borne plant pathogens’. pp. 174–176. (APS Press: St Paul)
Milligan SB,
Bodeau J,
Yaghoobi J,
Kaloshian IPZ, Williamson VM
(1998) The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. The Plant Cell 10, 1307–1319.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Morandi D,
Gollotte A, Camporota P
(2002) Influence of an arbuscular mycorrhizal fungus in the interaction of a binucleate Rhizoctonia species with Myc+ and Myc– pea roots. Mycorrhiza 12, 97–102.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nombela G,
Williamson VM, Muniz M
(2003) The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Molecular Plant–Microbe Interactions 16, 645–649.
| PubMed |
Parniske M
(2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Current Opinion in Plant Biology 7, 414–421.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Peterson, RL ,
and
Guinel, FC (2000). The use of plant mutants to study regulation of colonisation by AM fungi. In ‘Arbuscular mycorrhizas: physiology and function’. pp. 147–171. (Kluwer Academic Publishers: Dordrecht)
Phillips JM, Hayman DS
(1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55, 158–161.
Poulsen KH,
Nagy R,
Gao L-L,
Smith SE,
Bucher M,
Smith FA, Jakobsen I
(2005) Physiological and molecular evidence for Pi uptake via the symbiotic pathway in a reduced mycorrhizal colonisation mutation in tomato associated with a compatible fungus. New Phytologist 168, 445–454.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ruiz-Lozano JM,
Roussel H,
Gianinazzi S, Gianinazzi-Pearson V
(1999) Defence genes are differentially induced by a mycorrhizal fungus and Rhizobium sp. in wild-type and symbiosis-defective pea genotypes. Molecular Plant–Microbe Interactions 12, 976–984.
Sambrook, J ,
Fritsch, EF ,
and
Maniatis, T (1989).
Simon L,
Lalonde M, Bruns TD
(1992) Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Applied and Environmental Microbiology 58, 291–295.
| PubMed |
Smith, SE ,
and
Read, DJ (1997).
Smith SE,
Smith FA, Jakobsen I
(2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiology 133, 16–20.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stracke S,
Kistner C,
Yoshida S,
Mulder L, Sato S , et al.
(2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417, 959–962.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Weinhold, AR ,
and
Sinclair, JB (1996). Rhizoctonia solani: penetration, colonization and host response. In ‘ species: taxonomy, molecular biology, ecology, pathology and disease control.’ pp. 163–174. (Kluwer Academic Publishers: Dordrecht)
White, TJ ,
Bruns, T ,
Lee, S ,
and
Taylor, J (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In ‘PCR protocols. A guide to methods and applications’. pp. 315–322. (Academic Press: San Diego)
Xue L,
Charest PM, Jabaji-Hare SH
(1998) Systemic induction of peroxidases, 1,3-β-glucanases, chitinases and resistance in bean plants by binucleate Rhizoctonia species. Phytopathology 88, 359–365.
