Raffinose positively regulates maize drought tolerance by reducing leaf transpiration.
RAFFINOSE SYNTHASE
carbohydrate metabolism
drought stress
maize (Zea mays)
raffinose
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
04 2023
04 2023
Historique:
revised:
11
01
2023
received:
16
08
2022
accepted:
13
01
2023
medline:
29
3
2023
pubmed:
28
1
2023
entrez:
27
1
2023
Statut:
ppublish
Résumé
Drought stress is one of the major constraints of global crop production. Raffinose, a non-reducing trisaccharide, has been considered to regulate positively the plant drought stress tolerance; however, evidence that augmenting raffinose production in leaves results in enhanced plant drought stress tolerance is lacking. The biochemical mechanism through which raffinose might act to mitigate plant drought stress remains unidentified. ZmRAFS encodes Zea mays RAFFINOSE SYNTHASE, a key enzyme that transfers galactose from the galactoside galactinol to sucrose for raffinose production. Overexpression of ZmRAFS in maize increased the RAFS protein and the raffinose content and decreased the water loss of leaves and enhanced plant drought stress tolerance. The biomass of the ZmRAFS overexpressing plants was similar to that of non-transgenic control plants when grown under optimal conditions, but was significantly greater than that of non-transgenic plants when grown under drought stress conditions. In contrast, the percentage of water loss of the detached leaves from two independent zmrafs mutant lines, incapable of synthesizing raffinose, was greater than that from null segregant controls and this phenomenon was partially rescued by supplementation of raffinose to detached zmrafs leaves. In addition, while there were differences in water loss among different maize lines, there was no difference in stomata density or aperture. Taken together, our work demonstrated that overexpression of the ZmRAFS gene in maize, in contrast to Arabidopsis, increased the raffinose content in leaves, assisted the leaf to retain water, and enhanced the plant drought stress tolerance without causing a detectable growth penalty.
Substances chimiques
Raffinose
N5O3QU595M
Water
059QF0KO0R
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
55-67Informations de copyright
© 2023 Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Braun, D.M. & Slewinski, T.L. (2009) Genetic control of carbon partitioning in grasses: roles of sucrose transporters and tie-dyed loci in phloem loading. Plant Physiology, 149, 71-81.
Cacela, C. & Hincha, D.K. (2006) Monosaccharide composition, chain length and linkage type influence the interactions of oligosaccharides with dry phosphatidylcholine membranes. Biochimica et Biophysica Acta-Biomembranes, 1758, 680-691.
Chen, Y. & Mi, G. (2018) Physiological mechanisms underlying post-silking nitrogen use efficiency of high-yielding maize hybrids differing in nitrogen remobilization efficiency. Journal of Plant Nutrition and Soil Science, 181, 923-931.
Cho, M.J., Wu, E., Kwan, J., Yu, M., Banh, J., Linn, W. et al. (2014) Agrobacterium-mediated high-frequency transformation of an elite commercial maize (Zea mays L.) inbred line. Plant Cell Reports, 33, 1767-1777.
Egert, A., Eicher, B., Keller, F. & Peters, S. (2015) Evidence for water deficit-induced mass increases of raffinose family oligosaccharides (RFOs) in the leaves of three Craterostigma resurrection plant species. Frontiers in Physiology, 6, 206.
Egert, A., Keller, F. & Peters, S. (2013) Abiotic stress-induced accumulation of raffinose in Arabidopsis leaves is mediated by a single raffinose synthase (RS5, At5g40390). BMC Plant Biology, 13, 218.
Elango, D., Rajendran, K., Van der Laan, L., Sebastiar, S., Raigne, J., Thaiparambil, N.A. et al. (2022) Raffinose family oligosaccharides: friend or foe for human and plant health? Frontiers in Plant Science, 13, 829118.
Gangl, R., Behmuller, R. & Tenhaken, R. (2015) Molecular cloning of AtRS4, a seed specific multifunctional RFO synthase/galactosylhydrolase in Arabidopsis thaliana. Frontiers in Plant Science, 6, 789.
Gangl, R. & Tenhaken, R. (2016) Raffinose family oligosaccharides act as galactose stores in seeds and are required for rapid germination of Arabidopsis in the dark. Frontiers in Plant Science, 7, 1115.
Gu, L., Han, Z., Zhang, L., Downie, B. & Zhao, T. (2013) Functional analysis of the 5′ regulatory region of the maize GALACTINOL SYNTHASE2 gene. Plant Science, 213, 38-45.
Gu, L., Zhang, Y., Zhang, M., Li, T., Dirk, L.M., Downie, B. et al. (2016) ZmGOLS2, a target of transcription factor ZmDREB2A, offers similar protection against abiotic stress as ZmDREB2A. Plant Molecular Biology, 90, 157-170.
Hannah, M.A., Zuther, E., Buchel, K. & Heyer, A.G. (2006) Transport and metabolism of raffinose family oligosaccharides in transgenic potato. Journal of Experimental Botany, 57, 3801-3811.
Hsu, P.K., Dubeaux, G., Takahashi, Y. & Schroeder, J.I. (2021) Signaling mechanisms in abscisic acid-mediated stomatal closure. The Plant Journal, 105, 307-321.
Jaakola, L., Pirttila, A.M., Halonen, M. & Hohtola, A. (2001) Isolation of high quality RNA from bilberry (Vaccinium myrtillus L.) fruit. Molecular Biotechnology, 19, 201-203.
Jeffrey, G.A. & Huang, D.B. (1990) The hydrogen bonding in the crystal structure of raffinose pentahydrate. Carbohydrate Research, 206, 173-182.
Kuhn, C. (2003) A comparison of the sucrose transporter systems of different plant species. Plant Biology, 5, 215-232.
Kuhn, C. & Grof, C.P.L. (2010) Sucrose transporters of higher plants. Current Opinion in Plant Biology, 13, 287-298.
Lahuta, L.B., Pluskota, W.E., Stelmaszewska, J. & Szablinska, J. (2014) Dehydration induces expression of GALACTINOL SYNTHASE and RAFFINOSE SYNTHASE in seedlings of pea (Pisum sativum L.). Journal of Plant Physiology, 171, 1306-1314.
Li, S.H., Li, T.P., Kim, W.D., Kitaoka, M., Yoshida, S., Nakajima, M. et al. (2007) Characterization of raffinose synthase from rice (Oryza sativa L. var. Nipponbare). Biotechnology Letters, 29, 635-640.
Li, T., Zhang, Y., Liu, Y., Li, X., Hao, G., Han, Q. et al. (2020) Raffinose synthase enhances drought tolerance through raffinose synthesis or galactinol hydrolysis in maize and Arabidopsis plants. The Journal of Biological Chemistry, 295, 8064-8077.
Li, T., Zhang, Y., Wang, D., Liu, Y., Dirk, L.M.A., Goodman, J. et al. (2017) Regulation of seed vigor by manipulation of raffinose family oligosaccharides in maize and Arabidopsis thaliana. Molecular Plant, 10, 1540-1555.
Li, Z.H., Peng, J.Y., Wen, X. & Guo, H.W. (2013) ETHYLENE-INSENSITIVE3 is a senescence-associated Gene that accelerates age-dependent leaf senescence by directly repressing miR164 transcription in Arabidopsis. Plant Cell, 25, 3311-3328.
Lowe, K., Wu, E., Wang, N., Hoerster, G., Hastings, C., Cho, M.J. et al. (2016) Morphogenic regulators baby boom and Wuschel improve monocot transformation. Plant Cell, 28, 1998-2015.
Nemali, K.S., Bonin, C., Dohleman, F.G., Stephens, M., Reeves, W.R., Nelson, D.E. et al. (2015) Physiological responses related to increased grain yield under drought in the first biotechnology-derived drought-tolerant maize. Plant, Cell & Environment, 38, 1866-1880.
Nishizawa, A., Yabuta, Y. & Shigeoka, S. (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiology, 147, 1251-1263.
Nleya, T., Chungu, C. & Kleinjan, J. (2016) Chapter 5. In: Clay, D.E., Carlson, C.G., Clay, S.A. & Byamukama, E. (Eds) Corn growth and development. iGrow Corn: Best Management Practices. South Dakota State University.
Obata, T., Witt, S., Lisec, J., Palacios-Rojas, N., Florez-Sarasa, I., Yousfi, S. et al. (2015) Metabolite profiles of maize leaves in drought, heat, and combined stress field trials reveal the relationship between metabolism and grain yield. Plant Physiology, 169, 2665-2683.
Peterbauer, T., Mach, L., Mucha, J. & Richter, A. (2002) Functional expression of a cDNA encoding pea (Pisum sativum L.) raffinose synthase, partial purification of the enzyme from maturing seeds, and steady-state kinetic analysis of raffinose synthesis. Planta, 215, 839-846.
Porebski, S., Bailey, L.G. & Baum, B.R. (1997) Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Molecular Biology Reports, 15, 8-15.
Saravitz, D.M., Pharr, D.M. & Carter, T.E. (1987) Galactinol synthase activity and soluble sugars in developing seeds of four soybean genotypes. Plant Physiology, 83, 185-189.
Schneider, T. & Keller, F. (2009) Raffinose in chloroplasts is synthesized in the cytosol and transported across the chloroplast envelope. Plant & Cell Physiology, 50, 2174-2182.
Selvaraj, M.G., Ishizaki, T., Valencia, M., Ogawa, S., Dedicova, B., Ogata, T. et al. (2017) Overexpression of an Arabidopsis thaliana galactinol synthase gene improves drought tolerance in transgenic rice and increased grain yield in the field. Plant Biotechnology Journal, 15, 1465-1477.
Shinozaki, K. & Yamaguchi-Shinozaki, K. (2007) Gene networks involved in drought stress response and tolerance. Journal of Experimental Botany, 58, 221-227.
Sui, X.L., Meng, F.Z., Wang, H.Y., Wei, Y.X., Li, R.F., Wang, Z.Y. et al. (2012) Molecular cloning, characteristics and low temperature response of raffinose synthase gene in Cucumis sativus L. Journal of Plant Physiology, 169, 1883-1891.
Taji, T., Ohsumi, C., Iuchi, S., Seki, M., Kasuga, M., Kobayashi, M. et al. (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. The Plant Journal, 29, 417-426.
Tenorio Berrio, R., Nelissen, H., Inze, D. & Dubois, M. (2022) Increasing yield on dry fields: molecular pathways with growing potential. The Plant Journal, 109, 323-341.
Usha, B., Bordoloi, D. & Parida, A. (2015) Diverse expression of sucrose transporter gene family in Zea mays. Journal of Genetics, 94, 151-154.
Villaluenga, C.M., Wardenska, M., Pilarski, R., Bednarczyk, M. & Gulewicz, K. (2004) Utilization of the chicken embryo model for assessment of biological activity of different oligosaccharides. Folia Biol (Krakow), 52, 135-142.