Some relationships between the gas exchange, biochemistry and molecular biology of photosynthesis during leaf development of tomato plants after transfer to different carbon dioxide concentrations

Abstract

Tomato plants were exposed to four concentrations of CO2 (350, 700, 1050 or 1400 μmol CO2 mol−1) for 31 d. The light‐saturated rate of photosynthesis (A) of the unshaded fifth leaf was measured at either an ambient CO2 concentration of 350 μmol CO2 mol−1 [A (350)] or at the level of CO2 at which the plants were grown. The chloroplast protein composition and the level of transcripts of nuclear or plastid photosynthesis‐associated genes (PAGs), as well as the main carbohydrate content of the fifth leaf maintained horizontal and unshaded, were also measured during leaf development. At 60 and 95% leaf expansion, the A of high‐CO2‐grown plants measured at growth CO2 was higher than the A (350) of the plants grown at ambient CO2. However, in the fully mature leaves, A (growth CO2) declined linearly as growth CO2 concentration increased. The A (350) of plants exposed to elevated CO2 up to 60% leaf expanion had not acclimated to high CO2. At 95% leaf expansion, A (350) was lower in plants grown at high CO2. A versus CO2 (Ci) for mature leaves showed that A of the plants grown at high CO2 was lower over the entire range than that for plants grown at present ambient CO2 concentration. Lines fitted to the linear part of the A/Ci curves were concurrent at a Ci of 49μmol CO2 mol−1 and A=−1.21μmol CO2 m−2s−1. This Ct value is close to Λ* (46 μmol CO2 mol−1), the compensation point at 27°C calculated from the equation described in Brooks & Farquhar (1985, Planta 165, 397–406). This A is an estimate of respiration in the light (R1) and was not affected by acclimation to elevated CO2. Thylakoid proteins (photo‐system I core protein, D1 and D2 of the photosystem II core complex, cytochrome f) were all reduced by elevated CO2 only in the fully mature leaves (31d exposure), whereas the large and small subunits of Rubisco and Rubisco activase proteins had already declined after 22 d exposure. Transcript levels of the plastid‐encoded PAG (rbcL, psbA, psaA‐B) were reduced in the mature leaves by elevated CO2 when expressed on a total RNA basis, but they were not sensitive to elevated CO2 when expressed on a chloroplast 16S rRNA basis. However, rbcS, rca and cab mRNA transcripts were lower in the plants grown at high CO2 than in control plants after 22 d exposure when expressed on a nuclear rRNA basis. The loss of these nuclear PAGs was correlated with an accumulation of soluble sugars and starch.

An Arabidopsis mutant showing reduced feedback inhibition of photosynthesis

“…A number of studies showed a loss of Rubisco total activity in leaves which accumulated soluble carbohydrates (Krapp etaL, 1991(Krapp etaL, , 1993Stitt, 1991;Van Oosten and Besford, 1995). This reduction in Rubisco activity was the result of a similar loss of Rubisco protein (Krapp etaL, 1993;Van Oosten and Besford, 1995) which was concomitant with a reduction in RBCS transcript (Criqui etaL, 1992;Krapp et aL, 1993;Van Oosten and Besford, 1995) and a repression of the transcriptional activity of a RBCS promoter (Krapp et aL, 1993;Sheen, 1989). The repression of RBCSand other genes by carbohydrates suggests a common mechanism of control of nuclear genes coding for photosynthetic proteins (Jang and Sheen, 1994;Jang etaL, 1997;Sheen, 1989Sheen, , 1994.…”

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 decrease of Rubisco activity in elevated [CO 2 ] (see Introduction) is accompanied by a decrease of the transcripts for RbcS, Rubisco activase (Rca) and chlorophyll a binding protein (Cab) (Van Oosten et al 1994;Van Oosten & Besford 1995;Nie et al 1995;Cheng et al 1998). 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).…”

“…One is based on the idea that acclimation is due to sugar-mediated regulation of gene expression (Stitt 1991;Jang & Sheen 1994;Van Oosten & Besford 1996). Acclimation was reported to be accompanied by a decrease of the levels of transcripts for the nuclear-encoded small subunit of Rubisco (RbcS), chlorophyll binding protein (Cab) and Rubisco activase (Rca) in tomato, whereas several plastid-encoded transcripts including RbcL, psaA, psaB and psbA (encoding the large subunit of Rubisco and core proteins in photosystems I and II) did not decrease (Van Oosten et al 1994;Van Oosten & Besford 1995). Elevated [CO 2 ] has also been reported to lead to a decrease of RbcS transcript in wheat (Nie et al 1995), several crop plants (Moore, Palmquist & Seemann 1997) and Arabidopsis (Cheng et al 1998).…”

Effects of Short- and Long-Term Elevated CO2 on the Expression of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Genes and Carbohydrate Accumulation in Leaves of Arabidopsis thaliana (L.) Heynh.1

“…On average, leaf soluble sugars increase by 52% and starch content increases by 160% (Long and Drake, 1992;Webber et al, 1994). Growth at elevated CO 2 may also result in a large decline in Rubisco protein (up to 60%;Sage et al, 1989;Besford et al, 1990;RowlandBamford et al, 1991) and significant decreases in the transcript levels of genes encoding the small (rbcS) and large (rbcL) subunits of Rubisco (Nie et al, 1995a;Van Oosten and Besford, 1995). However, the metabolic signals and biochemical/molecular mechanisms underlying this acclimation to elevated CO 2 are not well understood.…”