Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-10T13:50:20.079Z Has data issue: false hasContentIssue false
  • English
  • Français

Sorting out the LeMANs: endo-β-mannanase genes and their encoded proteins in tomato

Published online by Cambridge University Press:  01 September 2007

Xuemei Gong  and
J. Derek Bewley
Xuemei Gong
Affiliation:
Department of Molecular and Cellular Biology, University of Guelph, Ontario, N1G 2W1, Canada
J. Derek Bewley*
Affiliation:
Department of Molecular and Cellular Biology, University of Guelph, Ontario, N1G 2W1, Canada
*
*Correspondence Fax: +1 519 837 2075 Email: dbewley@uoguelph.ca
Get access Rights & Permissions [Opens in a new window]

Abstract

Endo-β-mannanase (EC 3.2.1.78) is involved in the hydrolysis of mannan-type polysaccharides that are present in plant cell walls, especially those of the seed endosperm. The genes encoding the endo-β-mannanases have been studied extensively in tomato (Solanum lycopersicum), and five genes (LeMAN1, LeMAN2, LeMAN3, LeMAN4 and LeMAN5) and/or their products have been isolated and characterized. LeMAN1, LeMAN2 and LeMAN3 are expressed in tomato seeds, LeMAN4 in the fruit and LeMAN5 in the flower. LeMAN5 and LeMAN2 are now considered to be the same gene, and the former is re-designated as LeMAN2*. Transcripts of LeMANs 1, 2 and 3 are detected only in the endosperm of tomato seeds, and their synthesis is promoted by gibberellic acid. LeMAN4, in the fruit, occurs as LeMAN4a and LeMAN4i genes that encode an active or inactive form of endo-β-mannanase, respectively. LeMAN1–4 enzymes encoded by these genes share 80% similarity in amino acid sequence. In tomato, the leucine amino acid present near to the C-terminus of the endo-β-mannanase is the most important for achieving full activity of the enzyme.

Keywords

cell wallsendo-β-mannanaseendosperm, LeMAN genesreserve mobilizationseed germinationSolanum lycopersicumtomato
Type
Research Perspective
Information
Seed Science Research , Volume 17 , Issue 3 , September 2007 , pp. 143 - 154
Copyright
Copyright © Cambridge University Press 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abe, H., Urao, T., Ito, T., Seki, M., Shinozaki, K.andYamaguchi-Shinozaki, K. (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15, 63–78.CrossRefGoogle ScholarPubMed
Banik, M., Bourgault, R.andBewley, J.D. (2001) Endo-β-mannanase is present in an inactive form in ripening tomato fruits of the cultivar Walter. Journal of Experimental Botany 52, 105–111.CrossRefGoogle Scholar
Bate, N.andTwell, D. (1998) Functional architecture of a late pollen promoter: pollen-specific transcription is developmentally regulated by multiple stage-specific and co-dependent activator elements. Plant Molecular Biology 37, 859–869.CrossRefGoogle ScholarPubMed
Bewley, J.D. (1997) Breaking down the walls: a role for endo-β-mannanase in release from seed dormancy? Trends in Plant Science 2, 464–469.CrossRefGoogle Scholar
Bewley, J.D.andBlack, M. (1994) Seeds: Physiology of development and germination (2nd edition). New York, Plenum Press.CrossRefGoogle Scholar
Bewley, J.D.andReid, J.S.G. (1985) Mannans and glucomannans. pp. 289–304in Dey, P.M.; Dixon, R.A. (Eds) Biochemistry of storage carbohydrates in green plants. London, Academic Press.Google Scholar
Bewley, J.D., Burton, R.A., Morohashi, Y.andFincher, G.B. (1997) Molecular cloning of a cDNA encoding a (1 → 4)-β-mannan endohydrolase from the seeds of germinated tomato (Lycopersicon esculentum). Planta 203, 454–459.CrossRefGoogle Scholar
Bewley, J.D., Banik, M., Bourgault, R., Feurtado, J.A., Toorop, P.andHilhorst, H.W.M. (2000) Endo-β-mannanase activity increases in the skin and outer pericarp of tomato fruits during ripening. Journal of Experimental Botany 51, 529–538.CrossRefGoogle ScholarPubMed
Bourgault, R.andBewley, J.D. (2002) Variation in its C-terminal amino acids determines whether endo-β-mannanase is active or inactive in ripening tomato fruits of different cultivars. Plant Physiology 130, 1254–1262.CrossRefGoogle ScholarPubMed
Bourgault, R., Oakley, A.J., Bewley, J.D.andWilce, M.C.J. (2005) Three-dimensional structure of (1,4)-β-D-mannan mannanohydrolase from tomato fruit. Protein Science 14, 1233–1241.CrossRefGoogle ScholarPubMed
Bradford, K.J., Chen, F., Cooley, M.B., Dahal, P., Downie, B., Fukunaga, K.K., Gee, O.H., Gurusinghe, S., Mella, R.A., Wu, C.T., Yang, H.andYim, K.O. (2000) Gene expression prior to radicle emergence in imbibed tomato seeds. pp. 231–251in Black, M.; Bradford, K.J.; Vázquez-Ramos, J. (Eds) Seed biology: Advances and applications. Wallingford, CABI Publishing.Google Scholar
Carrington, C.M.S., Vendrell, M.andDomínguez-Puigjaner, E. (2002) Characterisation of an endo-(1,4)-β-mannanase (LeMAN4) expressed in ripening tomato fruit. Plant Science 163, 599–606.CrossRefGoogle Scholar
Chen, P.W., Chiang, C.M., Tseng, T.H.andYu, S.M. (2006) Interaction between rice MYBGA and the gibberellin response element controls tissue-specific sugar sensitivity of α-amylase genes. Plant Cell 18, 2326–2340.CrossRefGoogle ScholarPubMed
Christgau, S., Kauppinen, S., Vind, J., Kofod, L.V.andDalboge, H. (1994) Expression cloning, purification and characterization of a β-1,4-mannanase from Aspergillus aculeatus. Biochemistry and Molecular Biology International 33, 917–925.Google ScholarPubMed
Dahal, P.andBradford, K.J. (1990) Effects of priming and endosperm integrity on seed germination rates of tomato seeds: II. Germination at reduced water potential. Journal of Experimental Botany 41, 1441–1453.CrossRefGoogle Scholar
Da Silva, E.A.A., Toorop, P.E., van Aelst, A.C.andHilhorst, H.W.M. (2004) Abscisic acid controls embryo growth potential and endosperm cap weakening during coffee (Coffea arabica cv. Rubi) seed germination. Planta 220, 251–261.CrossRefGoogle ScholarPubMed
Dirk, L.M.A., Griffen, A.M., Downie, B.andBewley, J.D. (1995) Multiple isozymes of endo-β-mannanase in dry and imbibed seeds. Phytochemistry 40, 1045–1056.CrossRefGoogle Scholar
Downie, B., Hilhorst, H.W.M.andBewley, J.D. (1994) A new assay for quantifying endo-β-D-mannanase activity using Congo Red dye. Phytochemistry 36, 829–835.CrossRefGoogle Scholar
Downie, B., Hilhorst, H.W.M.andBewley, J.D. (1997) Endo-β-mannanase activity during dormancy alleviation and germination of white spruce (Picea glauca) seeds. Physiologia Plantarum 101, 405–415.CrossRefGoogle Scholar
Downie, B., Gurusinghe, S.andBradford, K.J. (1999) Internal anatomy of individual tomato seeds: relationship to abscisic acid and germination physiology. Seed Science Research 9, 117–128.CrossRefGoogle Scholar
Dulson, J.andBewley, J.D. (1989) Mannanase from Lactuca sativa: metabolic requirements for production and partial purification. Phytochemistry 28, 363–369.CrossRefGoogle Scholar
Dutta, S., Bradford, K.J.andNevins, D.J. (1994) Cell-wall autohydrolysis in isolated endosperms of lettuce (Lactuca sativa L.). Plant Physiology 104, 623–628.CrossRefGoogle ScholarPubMed
Eira, M.T.S., da Silva, E.A.A., de Castro, R.D., Dussert, S., Walters, C., Bewley, J.D.andHilhorst, H.W.M. (2006) Coffee seed physiology. Brazilian Journal of Plant Physiology 18, 149–163.CrossRefGoogle Scholar
Elmayan, T.andTepfer, M. (1995) Evaluation in tobacco of the organ specificity and strength of the rol D promoter, domain A of the 35S promoter and the 35S2 promoter. Transgenic Research 4, 388–396.CrossRefGoogle Scholar
Filichkin, S.A., Leonard, J.M., Monteros, A., Liu, P.P.andNonogaki, H. (2004) A novel endo-β-mannanase gene in tomato LeMAN5 is associated with anther and pollen development. Plant Physiology 134, 1080–1087.CrossRefGoogle ScholarPubMed
Fusada, N., Masuda, T., Kuroda, H., Shimada, H., Ohta, H.andTakamiya, K. (2005) Identification of a novel cis-element exhibiting cytokinin-dependent protein binding in vitro in the 5′-region of NADPH-protochlorophyllide oxidoreductase gene in cucumber. Plant Molecular Biology 59, 631–645.CrossRefGoogle ScholarPubMed
Goldberg, R.andRoland, J.C. (1971) Étude de l'utilization des glucomannans au cours de la germination des graines d'Asparagus officinalis. Révue Générale Botanique 78, 75–102.Google Scholar
Gong, X., Bassel, G.W., Wang, A., Greenwood, J.S.andBewley, J.D. (2005) The emergence of embryos from hard seeds is related to the structure of the cell walls of the micropylar endosperm, and not to endo-β-mannanase activity. Annals of Botany 96, 1165–1173.CrossRefGoogle Scholar
Groot, S.P.C.andKarssen, C.M. (1987) Gibberellins regulate seed germination in tomato by endosperm weakening: a study with gibberellin-deficient mutants. Planta 171, 525–531.CrossRefGoogle ScholarPubMed
Groot, S.P.C., Kieliszewska-Rokicka, B., Vermeer, E.andKarssen, C.M. (1988) Gibberellin-induced hydrolysis of endosperm cell walls in gibberellin-deficient tomato seeds prior to radicle protrusion. Planta 174, 500–504.CrossRefGoogle ScholarPubMed
Haigh, A.M.andBarlow, E.W.R. (1987) Water relations of tomato seed germination. Australian Journal of Plant Physiology 14, 485–492.Google Scholar
Halmer, P. (1989) De novo synthesis of mannanase by the endosperm of Lactuca sativa. Phytochemistry 28, 371–377.CrossRefGoogle Scholar
Halmer, P., Bewley, J.D.andThorpe, T.A. (1975) Enzyme to break down lettuce endosperm cell wall during gibberellin- and light-induced germination. Nature 258, 716–718.CrossRefGoogle Scholar
Halmer, P., Bewley, J.D.andThorpe, T.A. (1976) An enzyme to degrade lettuce endosperm cell walls: appearance of a mannanase following phytochrome- and gibberellin-induced germination. Planta 130, 189–196.CrossRefGoogle ScholarPubMed
Higo, K., Ugawa, Y., Iwamoto, M.andKorenaga, T. (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Research 27, 297–300.CrossRefGoogle ScholarPubMed
Homrichhausen, T.M., Hewitt, J.R.andNonogaki, H. (2003) Endo-β-mannanase activity is associated with the completion of embryogenesis in imbibed carrot (Daucus carota L.) seeds. Seed Science Research 13, 219–227.CrossRefGoogle Scholar
Kaplan, B., Davydov, O., Knight, H., Galon, Y., Knight, M.R., Fluhr, R.andFromm, H. (2006) Rapid transcriptome changes induced by cytosolic Ca2+ transients reveal ABRE-related sequences as Ca2+-responsive cis elements in Arabidopsis. Plant Cell 18, 2733–2748.CrossRefGoogle ScholarPubMed
Kelly, M.O.andBradford, K.J. (1986) Insensitivity of the Diageotropica tomato mutant to auxin. Plant Physiology 82, 713–717.CrossRefGoogle ScholarPubMed
Keusch, L. (1968) Die mobilisierung des reservemannans im keimenden Dattelsamen. Planta 78, 321–350.CrossRefGoogle Scholar
Kontos, F.andSpyropoulos, C.G. (1996) Effect of linoleic, linolenic and jasmonic acid on the production of α-galactosidase and endo-β-mannanase in the endosperms of carob and fenugreek seeds. Journal of Plant Physiology 149, 629–632.CrossRefGoogle Scholar
Lu, C.A., Ho, T.H.D., Ho, S.L.andYu, S.M. (2002) Three novel MYB proteins with one DNA binding repeat mediate sugar and hormone regulation of α-amylase gene expression. Plant Cell 14, 1963–1980.CrossRefGoogle ScholarPubMed
Malek, L.andBewley, J.D. (1991) Endo-β-mannanase activity and reserve mobilization in excised endosperms of fenugreek is affected by volume of incubation and abscisic acid. Seed Science Research 1, 45–49.CrossRefGoogle Scholar
Marraccini, P., Rogers, W.J., Allard, C., André, M-L., Caillet, V., Lacoste, N., Lausanne, F.andMichaux, S. (2001) Molecular and biochemical characterization of endo-β-mannanases from germinating coffee (Coffea arabica) grains. Planta 213, 296–308.CrossRefGoogle ScholarPubMed
McCleary, B.V. (1978) Purification of a β-mannanase enzyme from lucerne seed by substrate affinity chromatography. Phytochemistry 17, 651–653.CrossRefGoogle Scholar
McCleary, B.V. (1988) β-D-Mannanase. Methods in Enzymology 160, 596–610.CrossRefGoogle Scholar
McCleary, B.V.andMatheson, N.K. (1975) Galactomannan structure and β-mannanase and β-mannosidase activity in germinating legume seeds. Phytochemistry 14, 1187–1194.CrossRefGoogle Scholar
McClendon, J.H., Nolan, W.G.andWenzler, H.F. (1976) The role of the endosperm in the germination of legumes: galactomannan, nitrogen, and phosphorus changes in the germination of guar (Cyamopsis tetragonoloba; Leguminosae). American Journal of Botany 63, 790–797.CrossRefGoogle Scholar
Nakashima, K., Fujita, Y., Katsura, K., Maruyama, K., Narusaka, Y., Seki, M., Shinozaki, K.andYamaguchi-Shinozaki, K. (2006) Transcriptional regulation of ABI3- and ABA-responsive genes including RD29B and RD29A in seeds, germinating embryos, and seedlings of Arabidopsis. Plant Molecular Biology 60, 51–68.CrossRefGoogle ScholarPubMed
Nonogaki, H., Nomaguchi, M.andMorohashi, Y. (1995) Endo-β-mannanases in the endosperm of germinated tomato seeds. Physiologia Plantarum 94, 328–334.CrossRefGoogle Scholar
Nonogaki, H., Gee, O.H.andBradford, K.J. (2000) A germination-specific endo-β-mannanase is expressed in the micropylar endosperm cap of tomato seeds. Plant Physiology 123, 1235–1245.CrossRefGoogle ScholarPubMed
Ogawa, M., Hanada, A., Yamauchi, Y., Kuwahara, A., Kamiya, Y.andYamaguchi, S. (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15, 1591–1604.CrossRefGoogle ScholarPubMed
Pressey, R. (1989) Endo-β-mannanase in tomato fruit. Phytochemistry 28, 3277–3280.CrossRefGoogle Scholar
Reese, E.T.andShibata, Y. (1965) β-Mannananses of fungi. Canadian Journal of Microbiology 11, 167–183.CrossRefGoogle ScholarPubMed
Reid, J.S.G. (1971) Reserve carbohydrate metabolism in germinating seeds of Trigonella foenum-graecum L. (Leguminosae). Planta 100, 131–142.CrossRefGoogle ScholarPubMed
Reid, J.S.G.andMeier, H. (1970) Chemotaxonomic aspects of the reserve galactomannan in leguminous seeds. Zeitschrift für Pflanzenphysiologie 62, 89–92.Google Scholar
Reid, J.S.G.andMeier, H. (1972) The function of the aleurone layer during galactomannan mobilisation in germinating seeds of fenugreek (Trigonella foenum-graecum L.), crimson clover (Trifolium incarnatum L.) and lucerne (Medicago sativa L.): a correlative biochemical and ultrastructural study. Planta 106, 44–60.CrossRefGoogle ScholarPubMed
Reid, J.S.G.andMeier, H. (1973) Enzymic activities and galactomannan mobilization in germinating seeds of fenugreek Trigonella foenum-graecum L. Leguminosae. Secretion of α-galactosidase and β-mannosidase by the aleurone layer. Planta 112, 301–303.CrossRefGoogle Scholar
Ross, E.J.H., Stone, J.M., Elowsky, C.G., Arredondo-Peter, R., Klucas, R.V.andSarath, G. (2004) Activation of the Oryza sativa non-symbiotic haemoglobin-2 promoter by the cytokinin-regulated transcription factor, ARR1. Journal of Experimental of Botany 55, 1721–1731.CrossRefGoogle ScholarPubMed
Sánchez, R.A.andde Miguel, L. (1997) Phytochrome promotion of mannan-degrading enzyme activities in the micropylar endosperm of Datura ferox seeds requires the presence of embryo and gibberellin synthesis. Seed Science Research 7, 27–33.CrossRefGoogle Scholar
Sánchez, R.A., Sunell, L., Labavitch, J.M.andBonner, B.A. (1990) Changes in the endosperm cell walls of two Datura species before radicle protrusion. Plant Physiology 93, 89–97.CrossRefGoogle ScholarPubMed
Satoh, R., Nakashima, K., Seki, M., Shinozaki, K.andYamaguchi-Shinozaki, K. (2002) ACTCAT, a novel cis-acting element for proline- and hypoosmolarity-responsive expression of the ProDH gene encoding proline dehydrogenase in Arabidopsis. Plant Physiology 130, 709–719.CrossRefGoogle ScholarPubMed
Schröder, R., Wegrzyn, T.F., Sharma, N.N.andAtkinson, R.G. (2006) LeMAN4 endo-β-mannanase from ripe tomato fruit can act as a mannan transglycosylase or hydrolase. Planta 224, 1091–1102.CrossRefGoogle ScholarPubMed
Seiler, A. (1977) Galactomannan breakdown in germinating carob seeds (Ceratonia siliqua L.). Planta 134, 209–221.CrossRefGoogle ScholarPubMed
Sekhar, K.N.C.andDeMason, D.A. (1990) Identification and immunocytochemical localization of α-galactosidase in resting and germinated date palm (Phoenix dactylifera L.) seeds. Planta 181, 53–61.CrossRefGoogle ScholarPubMed
Shirsat, A., Wilford, N., Croy, R.andBoulter, D. (1989) Sequences responsible for the tissue specific promoter activity of a pea legumin gene in tobacco. Molecular and General Genetics 215, 326–331.CrossRefGoogle ScholarPubMed
Simpson, S.D., Nakashima, K., Narusaka, Y., Seki, M., Shinozaki, K.andYamaguchi-Shinozaki, K. (2003) Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. Plant Journal 33, 259–270.CrossRefGoogle ScholarPubMed
Stalberg, K., Ellerstom, M., Ezcurra, I., Ablov, S.andRask, L. (1996) Disruption of an overlapping E-box/ABRE motif abolished high transcription of the napA storage-protein promoter in transgenic Brassica napus seeds. Planta 199, 515–519.CrossRefGoogle ScholarPubMed
Sutoh, K.andYamauchi, D. (2003) Two cis-acting elements necessary and sufficient for gibberellin-upregulated proteinase expression in rice seeds. Plant Journal 34, 636–645.CrossRefGoogle ScholarPubMed
Toorop, P.E., Bewley, J.D.andHilhorst, H.W.M. (1996) Endo-β-mannanase isoforms are present in the endosperm and embryo of tomato seeds, but are not essentially linked to the completion of germination. Planta 200, 153–158.CrossRefGoogle Scholar
Toyofuku, K., Umemura, T.andYamaguchi, J. (1998) Promoter elements required for sugar-repression of the RAmy3D gene for α-amylase in rice. FEBS Letters 428, 275–280.CrossRefGoogle ScholarPubMed
Voigt, B.andBewley, J.D. (1996) Developing tomato seeds when removed from the fruit produce multiple forms of germinative and post-germinative endo-β-mannanase. Responses to desiccation, abscisic acid and osmoticum. Planta 200, 71–77.CrossRefGoogle Scholar
Wang, A., Li, J.andBewley, J.D. (2004) Molecular cloning and characterization of an endo-β-mannanase gene expressed in the lettuce endosperm following radicle emergence. Seed Science Research 14, 267–276.CrossRefGoogle Scholar
Wang, A., Wang, X., Ren, Y., Gong, X.andBewley, J.D. (2005) Endo-β-mannanase and β-mannosidase activities in rice grains during and following germination, and the influence of gibberellin and abscisic acid. Seed Science Research 15, 219–227.CrossRefGoogle Scholar
Williams, H.A., Bewley, J.D., Greenwood, J.S., Bourgault, R.andMo, B. (2001) The storage cell walls in the endosperm of Asparagus officinalis L. seeds during development and following germination. Seed Science Research 11, 305–315.Google Scholar
Yuan, J.S., Yang, X., Lai, J., Lin, H., Cheng, Z.-M., Nonogaki, H.andChen, F. (2007) The endo-β-mannanase gene families in Arabidopsis, rice and poplar. Function and Integrative Genomics 7, 1–16.CrossRefGoogle ScholarPubMed