Regulation of Cell-Specific Inositol Metabolism and Transport in Plant Salinity Tolerance

Abstract

myo-Inositol and its derivatives are commonly studied with respect to cell signaling and membrane biogenesis, but they also participate in responses to salinity in animals and plants. In this study, we focused on L -myo -inositol 1-phosphate synthase (INPS), which commits carbon to de novo synthesis, and myo -inositol O -methyltransferase (IMT), which uses myo -inositol for stress-induced accumulation of a methylinositol, D -ononitol. The Imt and Inps promoters are transcriptionally controlled. We determined that the transcription rates, transcript levels, and protein abundance are correlated. During normal growth, INPS is present in all cells, but IMT is repressed. After salinity stress, the amount of INPS was enhanced in leaves but repressed in roots. IMT was induced in all cell types. The absence of myo -inositol synthesis in roots is compensated by inositol/ononitol transport in the phloem. The mobilization of photosynthate through myo -inositol translocation links root metabolism to photosynthesis. Our model integrates the transcriptional control of a specialized metabolic pathway with physiological reactions in different tissues. The tissue-specific differential regulation of INPS, which leads to a gradient of myo -inositol synthesis, supports root growth and sodium uptake. By inducing expression of IMT and increasing myo -inositol synthesis, metabolic end products accumulate, facilitating sodium sequestration and protecting photosynthesis. INTRODUCTIONA central focus of our work is to determine genes that underlie mechanisms providing salinity tolerance in higher plants. In addition, we hope to learn how whole plants adapt metabolically. Many researchers have studied tolerance mechanisms in plants. Their findings show the importance of metabolite accumulation, which generally is attributed to osmotic adjustment leading to water retention and/or protection of biochemical pathways. When single enzymes were tested in transgenic plants, the accumulation of mannitol, proline, fructans, trehalose, glycine betaine, or ononitol (Tarczynski et al., 1993;Kavi Kishor et al., 1995;Pilon-Smits et al., 1995;Holmström et al., 1996;Hayashi et al., 1997;Sheveleva et al., 1997) provided marginally higher salinity and cold or drought tolerance. The manipulation of biochemical pathways by the transfer of multiple genes will be an even more appropriate strategy that is expected to provide broader tolerance because salinity tolerance is a multigenic trait Warne et al., 1995;Bohnert and Jensen, 1996). Salinity tolerance is also a multicellular trait, and the remodeling of complex pathways in transgenic plants will require knowledge of the distribution of such pathways throughout the plant. We have analyzed the myo -inositol biosynthetic pathway-leading to methylated inositols-that feeds into a pathway specific to salinity tolerance in a halophyte, the common ice plant ( Mesembryanthemum crystallinum ) (Loewus and Dickinson, 1982;Vernon and Bohnert, 1992).myo -Inositol is a central component of several biochemical pathways. It i...

Planteose is a short-term storage carbohydrate in Actinidia leaves

“…Osmoprotective functions of free myo-inositol have been demonstrated in plants (Sheveleva et al 1997;Nelson et al 1998;Klages et al 1999), with conclusive evidence recently demonstrated in transgenic tobacco (Majee et al 2004).…”

“…is the precursor to its methyl ethers that in turn, have been shown to accumulate in response to environmental stress as compatible solutes (Bohnert et al 1995;Ishitani et al 1996;Nelson et al 1998). Osmoprotective functions of free myo-inositol have been demonstrated in plants (Sheveleva et al 1997;Nelson et al 1998;Klages et al 1999), with conclusive evidence recently demonstrated in transgenic tobacco (Majee et al 2004).…”

A CAM- and starch-deficient mutant of the facultative CAM species Mesembryanthemum crystallinum reconciles sink demands by repartitioning carbon during acclimation to salinity

“…In M. crystallinum , the de novo synthesis of inositol (as a precursor to ononitol and pinitol) proceeds from glucose 6-phosphate through two steps catalysed by myo-inositol-1-phosphate synthase (INPS) and inositol monophosphatase (IMP; Nelson et al , 1998). Wild-type and mutant M. crystallinum accumulated similar amounts of cyclitols under salinity, indicating that starch mobilization is not required for the synthesis of these compatible solutes, which are thus likely to be derived from primary photosynthate and/or processing of the soluble sugar pool.…”

Perturbing the metabolic dynamics of myo-inositol in developing Brassica napus seeds through in vivo methylation impacts its utilization as phytate precursor and affects downstream metabolic pathways

“…The His-tagged protein was purified with Ni-NTA Agarose (Qiagen) under denaturing conditions. The purified protein (43 Kda) was used to raise polyclonal antibodies against the IMT enzyme [50], which were subsequently used in Western analyses of transgenic lines.…”