Response of mannitol-producing Arabidopsis thaliana to abiotic stress
Christine M. Sickler A , Gerald E. Edwards A , Olavi Kiirats A , Zhifang Gao B and Wayne Loescher B CA School of Biological Sciences and Center for Integrated Biotechnology, Washington State University, Pullman, WA 99164-4236, USA.
B Department of Horticulture, Michigan State University, East Lansing, MI 48824 1325, USA.
C Corresponding author. Email: loescher@msu.edu
D This paper originates from an International Symposium in Memory of Vincent R. Franceschi, Washington State University, Pullman, Washington, USA, June 2006.
Functional Plant Biology 34(4) 382-391 https://doi.org/10.1071/FP06274
Submitted: 27 October 2006 Accepted: 15 February 2007 Published: 19 April 2007
Abstract
In celery, mannitol is a primary photosynthetic product that is associated with celery’s exceptional salt tolerance. Arabidopsis plants transformed with celery’s mannose-6-phosphate reductase (M6PR) gene produce mannitol and grow normally in the absence of stress. Daily analysis of the increase in growth (fresh and dry weight, leaf number, leaf area per plant and specific leaf weight) over a 12-day period showed less effect of salt (100 mm NaCl) on the M2 transformant than wild type (WT). Following a 12-day treatment of WT, M2 and M5 plants with 100 or 200 mm NaCl the total shoot fresh weight, leaf number, and leaf area were significantly greater in transformants than in WT plants. The efficiency of use of energy for photochemistry by PSII was measured daily under growth conditions. In WT plants treated with 100 mm NaCl, the PSII yield begin decreasing after 6 days with a 50% loss in yield after 12 days, indicating a severe loss in PSII efficiency; whereas, there was no effect on the transformants. Under atmospheric levels of CO2, growth with 200 mm NaCl caused an increase in the substomatal levels of CO2 in WT plants but not in transformants. It also caused a marked decrease in carboxylation efficiency under limiting levels of CO2 in WT compared with transformants. When stress was imposed and growth reduced by withholding water for 12 days, which resulted in a similar decrease in relative water content to salt-treated plants, there were no differences among the genotypes in PSII yields or growth. The results suggest mannitol, which is known to be a compatible solute and antioxidant, protects photosynthesis against salt-related damage to chloroplasts.
Additional keywords: osmoprotectant, photosynthesis, salinity, salt, transgenic.
Acknowledgements
This study was supported in part by USDA CSREES Grant 2005-39454-16516 to WL and by NSF Grant IBN-0236959 to GE. We appreciate the help of Dr E. Voznesenskaya in preparation of the figures.
Abebe T,
Guenzi AC,
Martin B, Cushman JC
(2003) Tolerance of mannitol-accumulating transgenic wheat to water stress and salinity. Plant Physiology 131, 1748–1755.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Alia KY,
Sakamoto A,
Nonaka H,
Hayashi H,
Saradhi PP,
Chen THH, Murata N
(1999) Enhanced tolerance to light stress of transgenic Arabidopsis plants that express the codA gene for a bacterial choline oxidase. Plant Molecular Biology 40, 279–288.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Apse MP,
Aharon GS,
Snedden WA, Blumwald E
(1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiporter in Arabidopsis. Science 285, 1256–1258.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Aro E-M,
Virgin I, Andersson B
(1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochimica et Biophysica Acta 1143, 113–134.
| Crossref |
PubMed |
Bellaloui N,
Brown PH, Dandekar AM
(1999) Manipulation of in vivo sorbitol production alters boron uptake and transport in tobacco. Plant Physiology 119, 735–741.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bellaloui N,
Yadavc RC,
Chern M-S,
Hu H,
Gillen AM,
Greve C,
Dandekar AM,
Ronald PM, Brown PH
(2003) Transgenically enhanced sorbitol synthesis facilitates phloem-boron mobility in rice. Physiologia Plantarum 117, 79–84.
| Crossref | GoogleScholarGoogle Scholar |
Bohnert HJ, Jensen RG
(1996) Strategies for engineering water-stress tolerance in plants. Trends in Biotechnology 14, 89–97.
| Crossref | GoogleScholarGoogle Scholar |
Boyer JS
(1982) Plant productivity and environment. Science 218, 443–448.
| Crossref | GoogleScholarGoogle Scholar |
von Caemmerer S, Farquhar GD
(1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387.
| Crossref | GoogleScholarGoogle Scholar |
Chaturvedi V,
Bartiss A, Wong B
(1997) Expression of bacterial mtlD in Saccharomyces cerevisiae results in mannitol synthesis and protects a glycerol-defective mutant from high-salt and oxidative stress. Journal of Bacteriology 179, 157–162.
| PubMed |
Deguchi M,
Koshita Y,
Gao M,
Tao R,
Tetsumura T,
Yamaki S, Kanayama Y
(2004) Engineered sorbitol accumulation induces dwarfism in Japanese persimmon. Journal of Plant Physiology 161, 1177–1184.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Edwards GE, Baker NR
(1993) Can CO2 assimilation in maize leaves be predicted accurately from chlorophyll fluorescence analysis? Photosynthesis Research 37, 89–102.
| Crossref | GoogleScholarGoogle Scholar |
Everard JD,
Franceschi VR, Loescher WH
(1993) Mannose-6-phosphate reductase, a key enzyme in photoassimilate partitioning, is abundant and located in the cytosol of photosynthetically active cells of celery (Apium graveolens L.) source leaves. Plant Physiology 102, 345–356.
| PubMed |
Everard JD,
Gucci R,
Kann SC,
Flore JA, Loescher WH
(1994) Gas exchange and carbon partitioning in the leaves of celery (Apium graveolens L.) at various levels of root zone salinity. Plant Physiology 106, 281–292.
| PubMed |
Everard JD,
Cantini C,
Grumet R,
Plummer J, Loescher WH
(1997) Molecular cloning of mannose-6-phosphate reductase and its developmental expression in celery. Plant Physiology 113, 1427–1435.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Galinski EA
(1993) Compatible solutes of halophilic eubacteria: molecular principles, water-solute interaction, stress protection. Experientia 49, 487–496.
| Crossref | GoogleScholarGoogle Scholar |
Garg AK,
Kim JK,
Owens TG,
Ranwala AP,
Do Choi Y,
Kochian LV, Wu RJ
(2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proceedings of the National Academy of Sciences USA 99, 15 898–15 903.
| Crossref | GoogleScholarGoogle Scholar |
Gentry B,
Briantais J-M, Baker NR
(1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92.
Gigon A,
Matos A-R,
Laffray D,
Zuily-Fodil Z, Pham-Thi A-T
(2004) Effect of drought stress on lipid metabolism in the leaves of Arabidopsis thaliana (ecotype Columbia). Annals of Botany 94, 345–351.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hare PD,
Cress WA, Van Staden J
(1998) Dissecting the roles of osmolyte accumulation during stress. Plant, Cell & Environment 21, 535–553.
| Crossref | GoogleScholarGoogle Scholar |
Hayashi H,
Alia
,
Mustardy L,
Deshnium P,
Ida M, Murata N
(1997) Transformation of Arabidopsis thaliana with the codA gene for choline oxidase: accumulation of glycinebetaine and enhanced tolerance to salt and cold stress. Plant Journal 12, 133–142.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hu L,
Lu H,
Liu QL,
Chen XM, Jiang XN
(2005) Overexpression of mtlD gene in transgenic Populus tomentosa improves salt tolerance through accumulation of mannitol. Tree Physiology 25, 1273–1281.
| PubMed |
Jennings DB,
Ehrenshaft M,
Pharr DM, Williamson JD
(1998) Roles for mannitol and mannitol dehydrogenase in active oxygen-mediated plant defense. Proceedings of the National Academy of Sciences USA 95, 15 129–15 133.
| Crossref | GoogleScholarGoogle Scholar |
Jennings DB,
Daub ME,
Pharr DM, Williamson JD
(2002) Constitutive expression of a celery mannitol dehydrogenase in tobacco enhances resistance to the mannitol-secreting fungal pathogen Alternaria alternata. The Plant Journal 32, 41–49.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Karakas B,
Ozias-Akins P,
Stushnoff C,
Suefferheld M, Rieger R
(1997) Salinity and drought tolerance of mannitol-accumulating transgenic tobacco. Plant, Cell & Environment 20, 609–616.
| Crossref | GoogleScholarGoogle Scholar |
Krall JP, Edwards GE
(1992) Relationship between photosystem II activity and CO2 fixation in leaves. Physiologia Plantarum 86, 180–187.
| Crossref | GoogleScholarGoogle Scholar |
Laisk A, Loreto F
(1996) Determining photosynthetic parameters from leaf CO2 exchange and chlorophyll fluorescence. Plant Physiology 110, 903–912.
| PubMed |
Lal A,
Ku MSB, Edwards GE
(1996) Analysis of inhibition of photosynthesis due to water stress in the C3 species Hordeum vulgare and Vicia faba: electron transport, CO2 fixation and carboxylation capacity. Photosynthesis Research 49, 57–69.
| Crossref | GoogleScholarGoogle Scholar |
Lupinkova L, Komenda J
(2004) Oxidative modifications of the photosystem II D1 protein by reactive oxygen species: from isolated protein to cyanobacterial cells. Photochemistry and Photobiology 79, 152–162.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
McConnaughay KDM, Coleman JS
(1999) Biomass allocation in plants: ontogeny or optimality? A test along three resource gradients. Ecology 80, 2581–2593.
| Crossref | GoogleScholarGoogle Scholar |
Munns R
(2002) Comparative physiology of salt and water stress. Plant, Cell & Environment 25, 239–250.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nelson DE,
Rammesmayer G, Bohnert HJ
(1998) Regulation of cell-specific inositol metabolism and transport in plant salinity tolerance. The Plant Cell 10, 753–764.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pilon-Smits EH,
Ebskamp MM,
Paul MJ,
Jeuken MW,
Weisbeek PJ, Smeekens SM
(1995) Improved performance of transgenic fructan-accumulating tobacco under drought stress. Plant Physiology 107, 125–130.
| PubMed |
Rengel Z
(1992) The role of calcium in salt toxicity. Plant, Cell & Environment 15, 625–632.
| Crossref | GoogleScholarGoogle Scholar |
Romero C,
Bellees JM,
Vaya JL,
Serrano R, Culianez-Macia FA
(1997) Expression of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants: pleiotropic phenotypes include drought tolerance. Planta 201, 293–297.
| Crossref | GoogleScholarGoogle Scholar |
Rumpho ME,
Edwards GE, Loescher WH
(1983) A pathway for photosynthetic carbon flow to mannitol in celery leaves: activity and localization of key enzymes. Plant Physiology 73, 869–873.
| PubMed |
Sakamoto A, Murata N
(2002) The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant, Cell & Environment 25, 163–171.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sakamoto A,
Murata A, Murata N
(1998) Metabolic engineering of rice leading to biosynthesis of glycine betaine and tolerance to salt and cold. Plant Molecular Biology 38, 1011–1019.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shen B,
Jensen RG, Bohnert HJ
(1997a) Increased resistance to oxidative stress in transgenic plants by targeting mannitol biosynthesis to chloroplasts. Plant Physiology 113, 1177–1183.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shen B,
Jensen RG, Bohnert HJ
(1997b) Mannitol protects against oxidation by hydroxyl radicals. Plant Physiology 115, 527–532.
| PubMed |
Sheveleva E,
Marquez S,
Chmara W,
Zegeer A,
Jensen RG, Bohnert HJ
(1998) Sorbitol-6-phosphate dehydrogenase expression in transgenic tobacco. Plant Physiology 117, 831–839.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sheveleva EW,
Chmara W,
Bohnert HJ, Jensen RG
(1997) Increased salt and drought tolerance by D-ononitol production in transgenic Nicotiana tabacum L. Plant Physiology 115, 1211–1219.
| PubMed |
Shi H,
Lee B-H,
Wu S-J, Zhu JK
(2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nature 21, 81–85.
| Crossref | GoogleScholarGoogle Scholar |
Smirnoff N, Cumbes QJ
(1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28, 1057–1060.
| Crossref |
Tarczynski MC,
Jensen RG, Bohnert HJ
(1992) Expression of a bacterial mtlD gene in transgenic tobacco leads to production and accumlation of mannitol. Proceedings of the National Academy of Sciences USA 89, 2600–2604.
| Crossref | GoogleScholarGoogle Scholar |
Tarczynski MC,
Jensen RG, Bohnert HJ
(1993) Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science 259, 508–510.
| Crossref | GoogleScholarGoogle Scholar |
Thomas JC,
Sepahi M,
Arendall B, Bohnert HJ
(1995) Enhancement of seed germination in high salinity by engineering mannitol expression in Arabidopsis thaliana. Plant, Cell & Environment 18, 801–806.
| Crossref | GoogleScholarGoogle Scholar |
Vartanian N,
Marcotte L, Giraudat J
(1994) Drought rhizogenesis in Arabidopsis thaliana, differential response of hormonal mutants. Plant Physiology 104, 761–767.
| PubMed |
Vernon DM,
Tarczynski MC,
Jensen RG, Bohnert HJ
(1993) Cyclitol production in transgenic tobacco. The Plant Journal 4, 199–205.
| Crossref | GoogleScholarGoogle Scholar |
Williamson JD,
Jennings DB,
Guo W-E,
Pharr DM, Ehrenshaft M
(2002) Sugar alcohols, salt stress, and fungal resistance: polyols – multifunctional plant protection? Journal of the American Society for Horticultural Science 127, 467–473.
Zhifang G, Loescher WH
(2003) Expression of a celery mannose 6-phosphate reductase in Arabidopsis thaliana enhances salt tolerance and induces biosynthesis of both mannitol and a glucosyl-mannitol dimer. Plant, Cell & Environment 26, 275–283.
| Crossref | GoogleScholarGoogle Scholar |