Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Isolation and differential expression of β-1,3-glucanase messenger RNAs, SrGLU3 and SrGLU4, following inoculation of Sesbania rostrata

Chi-Te Liu A B , Toshihiro Aono A , Misako Kinoshita A , Hiroki Miwa A , Taichiro Iki A , Kyung-Bum Lee A and Hiroshi Oyaizu A
+ Author Affiliations
- Author Affiliations

A Laboratory of Plant Functional Biotechnology, Biotechnology Research Center, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan.

B Corresponding author. Email: aericliu@mail.ecc.u-tokyo.ac.jp

Functional Plant Biology 33(11) 983-990 https://doi.org/10.1071/FP06086
Submitted: 11 April 2006  Accepted: 27 June 2006   Published: 1 November 2006

Abstract

We report here the isolation and characterisation of two new β-1,3-glucanase cDNAs, SrGLU3 and SrGLU4, from a tropical legume Sesbania rostrata Bremek. & Oberm., which form N2-fixing nodules on the stem after infection by Azorhizobium caulinodans. SrGLU3 was characterised as being grouped in a branch with tobacco class I β-1,3-glucanases, where the isoforms were reported to be induced by either pathogen infection or ethylene treatment. SrGLU4 was characterised as separate from other classes, and we propose this new branch as a new class (Class VI). The SrGLU3 gene was constitutively expressed in normal stem nodules induced by the wild type strain of A. caulinodans (ORS571), and also even in immature stem nodules induced by a mutant (ORS571-C1), which could not form mature stem-nodules. In contrast, the transcript accumulation of SrGLU4 was hardly detectable in immature nodules inoculated by the ORS571-C1 mutant. We suggest that S. rostrata makes use of SrGLU4 to discriminate between symbionts and non-symbionts (mutants) in developing nodules. We propose the SrGLU4 gene as a new nodulin during nodulation.

Keywords: Azorhizobium caulinodans, β-1,3-glucanase, nodulation, pathogenesis-related (PR) protein, Sesbania rostrata, symbiosis, transcript accumulation.


Acknowledgments

This study is supported by Promotion of Basic Research Activities for Innovative Biosciences (PROBRAIN) of Bio-oriented Technology Research Advancement Institution (BRAIN) of Japan. We appreciate Dr Iain McTaggart (Department of Global Agricultural Sciences, The University of Tokyo) for his helpful suggestions and comments on the manuscript.


References


Akiyama T, Pillai MA, Sentoku N (2004) Cloning, characterization and expression of OsGLN2, a rice endo-1,3-β-glucanase gene regulated developmentally in flowers and hormonally in germinating seeds. Planta 220, 129–139.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Antoniw JF, Ritter CE, Pierpoint WS, Van Loon LC (1980) Comparison of three pathogenesis-related proteins from plants of two cultivars of tobacco infected with TMV. Journal of General Virology 47, 49–87. open url image1

Baron C, Zambryski PC (1995) The plant response in pathogenesis, symbiosis, and wounding: variations on a common theme? Annual Review of Genetics 29, 107–129.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bol JF, Linthorst HJM, Cornelissen BJC (1990) Plant pathogenesis-related proteins induced by virus infection. Annual Review of Phytopathology 28, 113–128.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bowles DJ (1990) Defence-related proteins in higher plants. Annual Review of Biochemistry 59, 873–907.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bucciaglia PA, Smith AG (1994) Cloning and characterization of Tag1, a tobacco anther β-1,3-glucanase expressed during tetrad dissolution. Plant Molecular Biology 24, 903–914.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Collinge DB, Kragh KM, Mikkelsen KN, Rasmussen U, Vad K (1993) Plant chitinases. The Plant Journal 3, 31–41.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cordero MJ, Raventos D, San Segundo B (1994) Differential expression and induction of chitinases and β-1,3-glucanases in response to fungal infection during germination of maize seeds. Molecular Plant–Microbe Interactions 7, 23–31. open url image1

Corich V, Goormachtig S, Lievens S, Van Montagu M, Holsters M (1998) Patterns of ENOD40 gene expression in stem-borne nodules of Sesbania rostrata. Plant Molecular Biology 37, 67–76.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cornelissen BJC, Melchers LS (1993) Strategies for control of fungal disease with transgenic plants. Plant Physiology 101, 709–712.
PubMed |
open url image1

D’Haeze W, Holsters M (2002) Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12, 79R–105R.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Djordjevic MA, Gabriel DW, Rolfe BG (1987) Rhizobium — the refined parasite of legumes. Annual Review of Phytopathology 25, 145–168.
Crossref | GoogleScholarGoogle Scholar | open url image1

Fanta N, Ortega X, Perez LM (2003) The development of Alternaria alternata is prevented by chitinases and β-1,3-glucanases from Citrus limon seedlings. Biological Research Journal 36, 411–420. open url image1

Felix G, Meins FJ (1986) Developmental and hormonal regulation of β-1,3-glucanase in tobacco. Planta 167, 206–211.
Crossref | GoogleScholarGoogle Scholar | open url image1

Goethals K, Leyman B, Van den Eede G, Van Montagu M, Holsters M (1994) An Azorhizobium caulinodans ORS571 locus involved in lipopolysaccharide production and nodule formation on Sesbania rostrata stems and roots. Journal of Bacteriology 176, 92–99.
PubMed |
open url image1

Goormachtig S, Alves-Ferreira M, Van Montagu M, Engler G, Holsters M (1997) Expression of cell cycle genes during Sesbania rostrata stem nodule development. Molecular Plant–Microbe Interactions 10, 316–325.
PubMed |
open url image1

Goormachtig S, Lievens S, Van de Velde W, Van Montagu M, Holsters M (1998) Srchi13, a novel early nodulin from Sesbania rostrata, is related to acidic class III chitinases. The Plant Cell 10, 905–916.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Goormachtig S, Van de Velde W, Lievens S, Verplancke C, Herman S, De Keyser A, Holsters M (2001) Srchi24, a chitinase homolog lacking an essential glutamic acid residue for hydrolytic activity, is induced during nodule development on Sesbania rostrata. Plant Physiology 127, 78–89.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Goormachtig S, Capoen W, Holsters M (2004) Rhizobium infection: lessons from the versatile nodulation behaviour of water-tolerant legumes. Trends in Plant Science 9, 518–522.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jin W, Horner HT, Palmer RG, Shoemaker RC (1999) Analysis and mapping of gene families encoding β-1,3-glucanases of soybean. Genetics 153, 445–452.
PubMed |
open url image1

Khan AA, Shi Y, Shih DS (2003) Cloning and partial characterization of a β-1,3-glucanase gene from strawberry. DNA Sequence 14, 406–412.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Knogge W, Kombrink E, Schmelzer E, Hahlbrock K (1987) Occurrence of phytoalexins and other putative defense-related substances in uninfected parsley plants. Planta 171, 279–287.
Crossref | GoogleScholarGoogle Scholar | open url image1

Leubner-Metzger G , Meins FJ (1999) Functions and regulation of plant β-1,3-glucanases PR-2. In ‘Pathogenesis-related proteins in plants’. (Eds SK Datta, S Mathukrishnan) pp. 49–76. (CRC Press: Boca Raton)

Leubner-Metzger G, Frundt C, Vogeli-Lange R, Meins FJ (1995) Class I β-1,3-glucanases in the endosperm of tobacco during germination. Plant Physiology 109, 751–759.
PubMed |
open url image1

Linthorst H, Melchers L, Mayer A, van Roekel J, Cornelissen B, Bol J (1990) Analysis of gene families encoding acidic and basic β-1,3-glucanases of tobacco. Proceedings of the National Academy of Sciences USA 87, 8756–8760.
Crossref | GoogleScholarGoogle Scholar | open url image1

Long SR, Staskawicz BJ (1993) Prokaryotic plant parasites. Cell 73, 921–935.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Macgregor EA, Ballance GM (1991) Possible secondary structure in plant and yeast β-glucanases. The Biochemical Journal 274, 41–44.
PubMed |
open url image1

Meins FJ , Neuhaus JM , Sperisen C , Ryals J (1992) The primary structure of plant pathogenesis-related glucanohydrolases and their genes. In ‘Genes involved in plant defense’. (Eds T Boller, FJ Meins) pp. 245–282. (Springer: Berlin)

Minami E, Kouchi H, Cohn JR, Ogawa T, Stacey G (1996a) Expression of the early nodulin, ENOD40, in soybean roots in response to various lipo-chitin signal molecules. The Plant Journal 10, 23–32.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Minami E, Kouchi H, Carlson RW, Cohn JR, Kolli VK, Day RB, Ogawa T, Stacey G (1996b) Cooperative action of lipo-chitin nodulation signals on the induction of the early nodulin, ENOD2, in soybean roots. Molecular Plant–Microbe Interactions 9, 574–583.
PubMed |
open url image1

Moore AE, Stone BA (1972) A β-1,3-glucan hydrolase from Nicotiana glutinosa. II. Specificity, action patterns and inhibitor studies. Biochimica et Biophysica Acta 258, 248–264.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research 8, 4321–4325.
PubMed |
open url image1

Mylona P, Pawlowski K, Bisseling T (1995) Symbiotic nitrogen fixation. The Plant Cell 7, 869–885.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Neale AD, Wahleithner JA, Lund M, Bonnett HT, Kelly A, Meeks-Wagner DR, Peacock WJ, Dennis ES (1990) Chitinase, β-1,3-glucanase, osmotin, and extensin are expressed in tobacco explants during flower formation. The Plant Cell 2, 673–684.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ori N, Sessa G, Lotan T, Himmelhoch S, Fluhr R (1990) A major stylar polypeptide sp41 is a member of the pathogenesis-related proteins superclass. EMBO Journal 9, 3429–3436.
PubMed |
open url image1

Payne G, Ward E, Gaffney T, Ahl Goy P, Moyer M (1990) Evidence for a third structural class of β-1,3-glucanase in tobacco. Plant Molecular Biology 15, 797–808.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Reddy PM, Ladha JK, Ramos MC, Maillet F, Hernandez RJ, Torrizo LB, Oliva NP, Datta SK, Datta K (1998) Rhizobial lipochitooligosaccharide nodulation factors activate expression of the legume early nodulin gene ENOD12 in rice. The Plant Journal 14, 693–702.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rezzonico E, Flury N, Meins FJ, Beffa R (1998) Transcriptional down-regulation by abscisic acid of pathogenesis-related β-1,3-glucanase genes in tobacco cell cultures. Plant Physiology 117, 585–592.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.
PubMed |
open url image1

Shinshi H, Wenzler H, Neuhaus JM, Felix G, Hofsteenge J, Meins F (1988) Evidence for N- and C-terminal processing of a plant defense-related enzyme: primary structure of tobacco prepro β-1,3-glucanase. Proceedings of the National Academy of Sciences USA 85, 5541–5545.
Crossref | GoogleScholarGoogle Scholar | open url image1

Suganuma N, Tamaoki M, Kouchi H (1995) Expression of nodulin genes in plant-determined ineffective nodules of pea. Plant Molecular Biology 28, 1027–1038.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
PubMed |
open url image1

Van den Bulcke M, Bauw G, Castresana C, Montagu MV, Vandekerckhove J (1989) Characterization of vacuolar and extracellular β-1,3-glucanases of tobacco: evidence for a strictly compartmentalized plant defense system. Proceedings of the National Academy of Sciences USA 86, 2673–2677.
Crossref | GoogleScholarGoogle Scholar | open url image1

Varghese JN, Garrett TPJ, Colman PM, Chen L, Hoj PB (1994) Three-dimensional structures of two plant β-glucan endohydrolases with distinct substrate specificities. Proceedings of the National Academy of Sciences USA 91, 2785–2789.
Crossref | GoogleScholarGoogle Scholar | open url image1

Vasse J, de Billy F, Truchet G (1993) Abortion of infection during the Rhizobium meliloti–alfalfa symbiotic interaction is accompanied by a hypersensitive reaction. The Plant Journal 4, 555–566.
Crossref | GoogleScholarGoogle Scholar | open url image1

Waterkeyn L (1981) Cytochemical localization and function of the 3-linked glucan callose in the developing cotton fiber cell wall. Protoplasma 106, 49–67.
Crossref | GoogleScholarGoogle Scholar | open url image1

Woloshuk C, Meulenhoff J, Sela-Buurlage M, Vandenelzen PJ, Cornelissen BJC (1991) Pathogen induced proteins with inhibitory activity towards Phytophthora infestans. The Plant Cell 3, 619–628.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wu C-T, Leubner-Metzger G, Meins F, Bradford KJ (2001) Class I β-1,3-glucanase and chitinase are expressed in the micropylar endosperm of tomato seeds prior to radicle emergence. Plant Physiology 126, 1299–1313.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Xi C, Lambrecht M, Vanderleyden J, Michiels J (1999) Bi-functional gfp- and gusA-containing mini-Tn5 transposon derivatives for combined gene expression and bacterial localization studies. Journal of Microbiological Methods 35, 85–92.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1