Expression of a Plant Cell Wall Invertase in Roots of Arabidopsis Leads to Early Flowering and an Increase in Whole Plant Biomass

Abstract

In order to enhance sink strength, we expressed a heterologous plant cell wall invertase (CrCIN1) under the control of a root-specific promoter (ppyk10) in Arabidopsis thaliana. Slightly elevated apoplastic invertase activity resulted in apparent phenotypic changes. Transgenic plants developed more secondary roots and subsequently, possibly because of a higher capacity to acquire nutrients, a higher shoot and whole plant biomass. Furthermore, an early flowering phenotype was detected. The data presented here demonstrate that it is possible to modulate carbohydrate metabolism by ectopic expression of cell wall invertases and thereby influence sink organ size and whole plant development.

Key words

Arabidopsis - cell wall invertase - sink strength - assimilate partitioning - flowering.

References

• 1 Balibrea Lara M. E., Gonzalez Garcia M. C., Fatima T., Ehness R., Lee T. K., Proels R., Tanner W., Roitsch T.. Extracellular invertase is an essential component of cytokinin-mediated delay of senescence.  Plant Cell. (2004);  16 1276-1287
• 2 Bürkle L., Hibberd J. M., Quick W. P., Kühn C., Hirner B., Frommer W. B.. The H⁺-sucrose cotransporter NtSUT1 is essential for sugar export from tobacco leaves.  Plant Physiology. (1998);  118 59-68
• 3 Bussis D., Heineke D., Sonnewald U., Willmitzer L., Raschke K., Heldt H. W.. Solute accumulation and decreased photosynthesis in leaves of potato plants expressing yeast-derived invertase either in the apoplast, vacuole or cytosol.  Planta. (1997);  202 126-136
• 4 Cheng W. H., Taliercio E. W., Chourey P. S.. The miniature1 seed locus of maize encodes a cell wall invertase required for normal development of endosperm and maternal cells in the pedicel.  Plant Cell. (1996);  8 971-983
• 5 Cho J. I., Lee S. K., Ko S., Kim H. K., Jun S. H., Lee Y. H., Bhoo S. H., Lee K. W., An G., Hahn T. R., Jeon J. S.. Molecular cloning and expression analysis of the cell-wall invertase gene family in rice (Oryza sativa L.).  Plant Cell Reports. (2005);  24 225-236
• 6 Clough S. J., Bent A. F.. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. .  The Plant Journal. (1998);  16 735-743
• 7 Gibeaut D. M., Hulett J., Cramer G. R., Seemann J. R.. Maximal biomass of Arabidopsis thaliana using a simple, low-maintenance hydroponic method and favorable environmental conditions.  Plant Physiology. (1997);  115 317-319
• 8 Dickinson C. C., Altabella T., Chrispeels M. J.. Slow-growth phenotype of transgenic tomato expressing apoplasmic invertase.  Plant Physiology. (1991);  95 420-425
• 9 Ehness R., Roitsch T.. Co-ordinated induction of mRNAs for extracellular invertase and a glucose transporter in Chenopodium rubrum by cytokinins.  The Plant Journal. (1997);  11 539-548
• 10 Eschrich W.. Phloem unloading of photoassimilates. Baker, D. A. and Milburn, J. A., eds. Transport of Photoassimilates. New York; Longman Scientific and Technical (1989): 206-263
• 11 Fotopoulos V., Gilbert M. J., Pittman J. K., Marvier A. C., Buchanan A. J., Sauer N., Hall J. L., Williams L. E.. The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atbetafruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. .  Plant Physiology. (2003);  132 821-829
• 12 Fridman E., Zamir D.. Functional divergence of a syntenic invertase gene family in tomato, potato, and Arabidopsis. .  Plant Physiology. (2003);  131 603-609
• 13 Godt D. E., Roitsch T.. Regulation and tissue-specific distribution of mRNAs for three extracellular invertase isoenzymes of tomato suggests an important function in establishing and maintaining sink metabolism.  Plant Physiology. (1997);  115 273-282
• 14 Goetz M., Godt D. E., Roitsch T.. Tissue-specific induction of the mRNA for an extracellular invertase isoenzyme of tomato by brassinosteroids suggests a role for steroid hormones in assimilate partitioning.  The Plant Journal. (2000);  22 515-522
• 15 Gottwald J. R., Krysan P. J., Young J. C., Evert R. F., Sussman M. R.. Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters.  Proceedings of the National Academy of Sciences of the USA. (2000);  97 13979-13984
• 16 Greiner S., Krausgrill S., Rausch T.. Cloning of a tobacco apoplasmic invertase inhibitor. Proof of function of the recombinant protein and expression analysis during plant development.  Plant Physiology. (1998);  116 733-742
• 17 Heineke D., Wildenberger K., Sonnewald U., Willmitzer L., Heldt H. W.. Accumulation of hexoses in leaf vacuoles: Studies with transgenic tobacco plants expressing yeast-derived invertase in the cytosol, vacuole or apoplasm.  Planta. (1994);  194 29-33
• 18 Heyer A. G., Raap M., Schroeer B., Marty B., Willmitzer L.. Cell wall invertase expression at the apical meristem alters floral, architectural, and reproductive traits in Arabidopsis thaliana. .  The Plant Journal. (2004);  39 161-169
• 19 Kim J. Y., Mahe A., Guy S., Brangeon J., Roche O., Chourey P. S., Prioul J. L.. Characterization of two members of the maize gene family, Incw3 and Incw4, encoding cell-wall invertases.  Gene. (2000);  245 89-102
• 20 Kühn C., Quick W. P., Schulz A., Riesmeier J. W., Sonnewald U., Frommer W. B.. Companion cell-specific inhibition of the potato sucrose transporter SUT1.  Plant, Cell and Environment. (1996);  19 1115-1123
• 21 Lemoine R., Kühn C., Thiele N., Delrot S., Frommer W. B.. Antisense inhibition of the sucrose transporter: effects on amount of carrier and sucrose transport activity.  Plant, Cell and Environment. (1996);  19 1124-1131
• 22 Miller M. E., Chourey P. S.. The maize invertase-deficient miniature-1 seed mutation is associated with aberrant pedicel and endosperm development.  Plant Cell. (1992);  4 297-305
• 23 Neubohn B., Gubatz S., Wobus U., Weber H.. Sugar levels altered by ectopic expression of a yeast-derived invertase affect cellular differentiation of developing cotyledons of Vicia narbonensis L. .  Planta. (2000);  211 325-334
• 24 Nitz I., Berkefeld H., Puzio P. S., Grundler F. M.. Pyk10, a seedling and root specific gene and promoter from Arabidopsis thaliana. .  Plant Science. (2001);  161 337-346
• 25 Rausch T., Greiner S.. Plant protein inhibitors of invertases.  Biochimica et Biophysica Acta. (2004);  1696 253-261
• 26 Riesmeier J. W., Willmitzer L., Frommer W. B.. Evidence for an essential role of the sucrose transporter in phloem loading and assimilate partitioning.  The EMBO Journal. (1994);  13 1-7
• 27 Roitsch T., Bittner M., Godt D. E.. Induction of apoplastic invertase of Chenopodium rubrum by D-glucose and a glucose analog and tissue-specific expression suggest a role in sink-source regulation.  Plant Physiology. (1995);  108 285-294
• 28 Ruan Y. L., Patrick J. W.. The cellular pathway of post-phloem sugar transport in developing tomato fruit.  Planta. (1995);  196 434-444
• 29 Sauer N., Friedlander K., Gräml-Wicke U.. Primary structure, genomic organization and heterologous expression of a glucose transporter from Arabidopsis thaliana. .  The EMBO Journal. (1990);  9 3045-3050
• 30 Scholz-Starke J., Büttner M., Sauer N.. AtSTP6, a new pollen-specific H⁺-monosaccharide symporter from Arabidopsis. .  Plant Physiology. (2003);  131 70-77
• 31 Sherson S. M., Alford H. L., Forbes S. M., Wallace G., Smith S. M.. Roles of cell-wall invertases and monosaccharide transporters in the growth and development of Arabidopsis. .  Journal of Experimental Botany. (2003);  54 525-531
• 32 Sherson S. M., Hemmann G., Wallace G., Forbes S., Germain V., Stadler R., Bechtold N., Sauer N., Smith S. M.. Monosaccharide/proton symporter AtSTP1 plays a major role in uptake and response of Arabidopsis seeds and seedlings to sugars.  The Plant Journal. (2000);  24 849-857
• 33 Sonnewald U., Brauer M., von Schaewen A., Stitt M., Willmitzer L.. Transgenic tobacco plants expressing yeast-derived invertase in either the cytosol, vacuole or apoplast: a powerful tool for studying sucrose metabolism and sink/source interactions.  The Plant Journal. (1991);  1 95-106
• 34 Sonnewald U.. Expression of E. coli inorganic pyrophosphatase in transgenic plants alters photoassimilate partitioning.  The Plant Journal. (1992);  2 571-581
• 35 Sonnewald U., Hajirezaei M. R., Kossmann J., Heyer A., Trethewey R. N., Willmitzer L.. Increased potato tuber size resulting from apoplastic expression of a yeast invertase.  Nature Biotechnology. (1997);  15 794-797
• 36 Tang G. Q., Luscher M., Sturm A.. Antisense repression of vacuolar and cell wall invertase in transgenic carrot alters early plant development and sucrose partitioning.  Plant Cell. (1999);  11 177-189
• 37 Truernit E., Schmid J., Epple P., Illig J., Sauer N.. The sink-specific and stress-regulated Arabidopsis STP4 gene: enhanced expression of a gene encoding a monosaccharide transporter by wounding, elicitors, and pathogen challenge.  Plant Cell. (1996);  8 2169-2182
• 38 Turgeon R.. The sink-source transition in leaves.  Annual Review of Plant Physiology and Plant Molecular Biology. (1989);  40 119-138
• 39 Tymowska-Lalanne Z., Kreis M.. Expression of the Arabidopsis thaliana invertase gene family.  Planta. (1998);  207 259-265
• 40 von Schaewen A., Stitt M., Schmidt R., Sonnewald U., Willmitzer L.. Expression of a yeast-derived invertase in the cell wall of tobacco and Arabidopsis plants leads to accumulation of carbohydrate and inhibition of photosynthesis and strongly influences growth and phenotype of transgenic tobacco plants.  The EMBO Journal. (1990);  9 3033-3044
• 41 Weber H., Buchner P., Borisjuk L., Wobus U.. Sucrose metabolism during cotyledon development of Vicia faba L. is controlled by the concerted action of both sucrose-phosphate synthase and sucrose synthase: expression patterns, metabolic regulation and implications for seed development.  The Plant Journal. (1996);  9 841-850
• 42 Weber H., Borisjuk L., Heim U., Sauer N., Wobus U.. A role for sugar transporters during seed development: molecular characterization of a hexose and a sucrose carrier in fava bean seeds.  Plant Cell. (1997);  9 895-908
• 43 Weber H., Heim U., Golombek S., Borisjuk L., Manteuffel R., Wobus U.. Expression of a yeast-derived invertase in developing cotyledons of Vicia narbonensis alters the carbohydrate state and affects storage functions.  The Plant Journal. (1998);  16 163-172
• 44 Weil M., Rausch T.. Cell wall invertase in tobacco crown gall cells: enzyme properties and regulation by auxin.  Plant Physiology. (1990);  94 1575-1578
• 45 Zuther E., Kwart M., Willmitzer L., Heyer A. G.. Expression of a yeast-derived invertase in companion cells results in long-distance transport of a trisaccharide in an apoplastic loader and influences sucrose transport.  Planta. (2004);  218 759-766

Editor: A. Weber