The sugar‐mediated regulation of genes encoding the small subunit of Rubisco and the regulatory subunit of ADP glucose pyrophosphorylase is modified by phosphate and nitrogen

Abstract

Tobacco seedlings were grown in nutrient agar at a range of ammonium nitrate concentrations either without added sucrose, or with 100 mol m -3 sucrose. In the absence of added sucrose, nitrogen-limited plants had increased levels of glucose, fructose and sucrose, decreased chlorophyll, decreased protein, and decreased Rubisco activity, but the level of the transcript for the small subunit of Rubisco (RbcS) did not decrease compared with nitrogen-sufficient plants. When sucrose was added to nitrogen-sufficient seedlings, there was an increase of sucrose, glucose and fructose in the leaves, growth was increased, and the chlorophyll and protein content, Rubisco activity, and the RbcS transcript level did not change. When sucrose was added to nitrogen-limited seedlings, there was a further increase of sucrose, glucose and fructose, growth was not increased, and there was a further decrease of chlorophyll, protein and Rubisco activity, and a marked decrease of the RbcS transcript level. To check that the decrease of the RbcS transcript level was not an indirect effect due to changes of nitrogen metabolites after adding sugars, glucose was added to Chenopodium cells in the presence and absence of glutamine or azaserine. Changes of glutamine that suffice to increase and decrease the level of the transcript for nitrate reductase (Nia) do not affect the RbcS transcript concentration, and glucose addition still led to a decrease of the RbcS transcript level when the internal glutamine concentration was high. Tobacco seedlings were also grown in nutrient agar at a range of phosphate concentrations either without added sucrose, or with 100 mol m -3 sucrose. Phosphate-limited seedlings did not show a decrease of chlorophyll, protein, Rubisco activity, or the level of the RbcS transcript, compared with phosphate-sufficient seedlings. The addition of sucrose to phosphate-limited plants led to a similar increase of sugars to that seen after adding sucrose to nitrogen-limited seedlings, but did not alter chlorophyll, protein, Rubisco activity, or the level of the RbcS transcript. The addition of sucrose to phosphate-limited plants led to a slight increase of the level of the transcript for nitrate reductase (Nia), increased nitrate reductase activity, and a marked increase of the amino acid content. Phosphate limitation led to an increased level of the transcript for the regulatory subunit of ADP glucose pyrophosphorylase (AgpS2), and this response was strengthened when sucrose was added. The regulation of AgpS2 expression by phosphate and sucrose was further investigated by feeding sucrose and phosphate to detached source leaves via the transpiration stream. The level of the AgpS2 transcript decreased after feeding phosphate and increased after feeding sucrose, and the effect of sucrose was antagonised by phosphate. It is concluded that the response to sugar signalling is modulated by nitrogen and phosphate in a gene-specific manner. The significance of these results for understanding the visual phenotype of nitrogen-and phospha...

The nitrate and ammonium nitrate supply have a major influence on the response of photosynthesis, carbon metabolism, nitrogen metabolism and growth to elevated carbon dioxide in tobacco

“…A similar decrease of Rubisco activity and of the levels of the transcripts for RbcS, Cab, and other photosynthesis proteins occurs when sugars accumulate in leaves as a result of an inhibition of phloem transport in a wide range of transgenic plants (Von Schaewen et al 1991;Krapp et al 1993;Riesmeier, Willmitzer & Frommer 1994;Geigenberger et al 1996), after petiole cooling (Krapp & Stitt 1995), and after sugar feeding (Krapp et al 1993;Paul & Stitt 1993;Van Oosten & Besford 1995;Nielsen et al 1998). This similarity prompted the hypothesis that the acclimation of photosynthesis to enhanced [CO 2 ] might be due to a sugar-mediated repression of RbcS and other genes involved in photosynthesis (Stitt 1991;see also Van Osten & Besford 1996).…”

“…The changes in partitioning are paralleled by changes in the level of the AgpS transcript, which encodes the regulatory subunit of AGPase, the key regulatory enzyme for starch synthesis. It is known that the AgpS transcript level can be increased by feeding sugars to detached leaves (Müller-Röber et al 1990;Nielsen et al 1998) and seedlings (Nielsen et al 1998), and by petiole cooling (Krapp & Stitt 1995). The increase of AgpS transcript in enhanced [CO 2 ] in nitrogen-sufficient plants might therefore be due to sugar-mediated regulation of AgpS expression.…”

“…The effect of nitrogen on acclimation could be explained if the sugar-mediated repression of RbcS and other photosynthesis proteins were to operate more effectively in nitrogen-limited plants, either because leaf carbohydrates are already higher and/or due to cross talk between sugar-and nitrogen-signalling systems. In agreement, the decline of Rubisco activity following nitrogen removal can be prevented if the plants are simultaneously transferred to low light (Paul & Driscoll 1997), and the addition of sugar to young plantlets leads to a marked decrease of RbcS transcript, Rubisco, protein and chlorophyll when they are nitrogen-limited whereas it leads to increased growth and has no effect on Rubisco activity, protein, chlorophyll and the RbcS transcript when they are nitrogen-replete (Paul & Stitt 1993;Nielsen et al 1998). An alternative explanation for the marked acclimation in nitrogen-limited plants, however, would be that the reallocation of nitrogen from old to young leaves is accelerated in elevated [CO 2 ], because the plants are larger and therefore experience an earlier or more acute nitrogen limitation (Coleman et al 1993;Nie et al 1995).…”

Physiological and molecular alterations in plants exposed to high [CO2] under phosphorus stress

“…For instance, limited P supply inhibits leaf growth which consequently results in overall plant growth reduction (Fredeen et al, 1989;Jeschke et al, 1996;Nielsen et al, 1998;Rodríguez et al, 1998;Mollier and Pellerin 1999;Chiera et al, 2002). These reductions are the consequence of lower rates of leaf initiation, less dividing cells, as well as reduced leaf expansion (Rodríguez et al, 1998;Rodrıǵuez et al, 2000;Plénet et al, 2000;Chiera et al, 2002;Assuero et al, 2004) (Fig.…”

Earthworms influence the production of above- and belowground biomass and the expression of genes involved in cell proliferation and stress responses in Arabidopsis thaliana

“…It is noteworthy that high levels of PLD gene expression have been observed in dividing and growing plant cells suggesting that it may play an essential role in cell proliferation (Xu et al, 1997). The RubcS transcripts that encode the small sub-unit of the ribulose 1,5-diphosphate carboxylase were studied here to assess the possible transcriptional impact of earthworms on the carbon fixing enzyme (Nielsen et al, 1998).…”