Sugar Regulates mRNA Abundance of H+-ATPase Gene Family Members in Tomato

Abstract

l h e plant plasma membrane H+-ATPase energizes the secondary uptake of nutrients and may facilitate cell expansion by acidifying the cell wall. In yeast, Clc stimulates the accumulation of H+-ATPase mRNA, and the growth rate supported by various sugars is correlated with H+-ATPase protein abundance. Expression of three H+-ATPase genes, LHAI, LHA2, and LHA4, was previously detected in tomato (Lycopersicon esculentum). We have characterized the sequence of the LHA4 gene and examined the expression of these three tomato H+-ATPase genes in growing tissues and i n response to exogenous sugars. LHA4 is a member of the H+-ATPase subfamily, including the Arabidopsis fhaliana genes AHAl, AHA2, and AHA3. l h e 5' untranslated region of the deduced LHA4 cDNA contains a short, open reading frame very similar to that in the Nicofiana plumbaginifolia gene PMAl . LHA4 transcript abundance in seedlings is correlated with cell growth, being 2.5 times greater in hypocotyls of dark-versus light-grown plants. The accumulation of both LHA4 and LHA2 mRNAs is induced by the addition of exogenous sugars and this induction appears to be dependent on sugar uptake and metabolism, because mannitol and 3-Omethylglucose do not stimulate mRNA accumulation. These results suggest that the induction of expression of H+-ATPase genes by metabolizable sugars may be part of a generalized cellular response to increased cell growth and metabolism promoted by the availability of an abundant carbon source.H+-ATPases in the PM plays a critica1 role in the physiology of plants at both the cellular and organismal levels. They establish an electrical potential and pH gradient across the PM, which provides the force for the secondary transport of anions, cations, amino acids, and sugars (Serrano, 1989;Sussman and Harper, 1989). These secondary transport systems control physiological processes such as nutrient uptake by roots, phloem transport, and stomatal function. H+-ATPase in the PM may have other physiological roles, because the enzyme is subjected to control by physiological effectors such as hormones, light, and pathogens (Serrano, 1989;Sussman and Harper, 1989 control of the cell cycle by the regulation of cytosolic pH (Pichon and Desbiez, 1994) and by driving the auxin-induced cell expansion by cell-wall acidification (Rayle and Cleland, 1992). Total H+-ATPase levels in the PM may be directly correlated with growth. Hager et al. (1991) demonstrated by immunodetection that H+-ATPase levels in the PM increased 2-fold during auxin-induced maize coleoptile elongation. Rao et al. (1993) showed that the growth rate of liquid cultures of yeast supported by different sugars is closely correlated with PM H+-ATPase activity. Furthermore, the expression of the primary yeast PM H+-ATPase isoform PMAl was shown to be induced by the addition of growth-inducing exogenous sugars.Considerable progress has recently been made in the understanding of the molecular biology of plant PM H+-ATPases. Multiple genes encoding PM H+-ATPases have been cloned in tomato (Lycopers...

Regulation of Root Ion Transporters by Photosynthesis: Functional Importance and Relation with Hexokinase

“…This finding suggests that the control exerted by light and sugars is a key regulatory process for transporter or channel proteins in the roots. This conclusion agrees with observations made in shoots that light regulates two H ϩ -ATPase genes (of three investigated) in tomato (Mito et al, 1996) and all four K ϩ channels identified in the pulvinus of the legume Samanea saman (Moshelion et al, 2002). Second, a strong correlation was found between the responses of transcript accumulation to illumination of the plant on the one hand and to sucrose supply to the roots on the other hand (Figure 3).…”

Symbiotic Status, Phosphate, and Sucrose Regulate the Expression of Two Plasma Membrane H+-ATPase Genes from the Mycorrhizal Fungus Glomus mosseae

“…Glc did not have any effect on the expression of either H ϩ -ATPase gene during presymbiosis, in contrast to what was observed for plants and yeast (Mito et al, 1996;Portillo, 2000). The effect of Glc on H ϩ -ATPase gene expression in other fungi has been found to be variable.…”

Calcium Signals: The Lead Currency of Plant Information Processing

“…Enhanced Ca 2+ extrusion was reported to occur in senescent potato (Solanum tuberosum; Fakhrai and Hall, 1984). Moreover, enhanced transcription of ATPases was observed in response to ABA (Cerana et al, 2006), sugar (Mito et al, 1996), or by sodium (Wimmers et al, 1992).…”