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

Abstract

To investigate the proposed molecular characteristics of sugarmediated repression of photosynthetic genes during plant acclimation to elevated CO 2 , we examined the relationship between the accumulation and metabolism of nonstructural carbohydrates and changes in ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) gene expression in leaves of Arabidopsis thaliana exposed to elevated CO 2 . Long-term growth of Arabidopsis at high CO 2 (1000 L L ؊1 ) resulted in a 2-fold increase in nonstructural carbohydrates, a large decrease in the expression of Rubisco protein and in the transcript of rbcL, the gene encoding the large subunit of Rubisco (approximately 35-40%), and an even greater decline in mRNA of rbcS, the gene encoding the small subunit (approximately 60%). This differential response of protein and mRNAs suggests that transcriptional/posttranscriptional processes and protein turnover may determine the final amount of leaf Rubisco protein at high CO 2 . Analysis of mRNA levels of individual rbcS genes indicated that reduction in total rbcS transcripts was caused by decreased expression of all four rbcS genes. Short-term transfer of Arabidopsis plants grown at ambient CO 2 to high CO 2 resulted in a decrease in total rbcS mRNA by d 6, whereas Rubisco content and rbcL mRNA decreased by d 9. Transfer to high CO 2 reduced the maximum expression level of the primary rbcS genes (1A and, particularly, 3B) by limiting their normal pattern of accumulation through the night period. The decreased nighttime levels of rbcS mRNA were associated with a nocturnal increase in leaf hexoses. We suggest that prolonged nighttime hexose metabolism resulting from exposure to elevated CO 2 affects rbcS transcript accumulation and, ultimately, the level of Rubisco protein.

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

“…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).…”

“…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). 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.…”

“…This phenomenon is termed photosynthetic 'acclimation'. Acclimation is accompanied by alterations in gas exchange characteristics that are indicative of a decreased capacity for carboxylation (Stitt 1991;Sage 1994) and by a decrease of Rubisco activity in tobacco Sicher, Kremer & Rodermel 1994), tomato (Van Oosten, Wilkins & Besford 1994), Arabidopsis (Cheng, Moore & Seeman 1998), Scirpus olneyi (Jacob et al 1995), wheat (Nie et al 1995;Rogers et al 1996b;Sicher & Bunce 1997), barley (Sicher & Bunce 1997), rice (Vu et al 1997), Panicum laxum (Ghannoum et al 1997), loblolly pine (Tissue, Thomas & Strain 1993, 1997, cherry (Atkinson et al (1997), oak (George, Gerant & Dizengremel 1996) and cork oak (Faria et al 1996). Acclimation of photosynthetic rate (Wong 1979;Oberbauer et al 1986;Tissue et al 1993;Pettersson et al 1993;Sage 1994;Pettersson & MacDonald 1994;El-Kohen & Mousseau 1994;Miglietta, Giuntoli & Bindi 1996;Rogers et al 1998) and the decrease of Rubisco activity in elevated [CO 2 ] (Wong 1979;Tissue et al 1993;Delgrado et al 1994;Webber, Nie & Long 1994;Riviere-Rolland, Contard & Betsche 1996;Rogers et al 1996a) is more marked in nitrogen-limited than in nitrogen-sufficient plants.…”

Ethylene Insensitivity Results in Down-Regulation of Rubisco Expression and Photosynthetic Capacity in Tobacco

“…Long-term growth at elevated CO 2 , for example, generally increases soluble sugar concentration in leaves (Van Oosten and Besford, 1994;Cheng et al, 1998). Such leaves often have lower Rubisco transcript levels and decreased photosynthetic capacity (Krapp et al, 1993;Besford, 1994, 1995;Cheng et al, 1998). Additional proof of down-regulation of the photosynthetic machinery by sugars came from cold-girdling petioles to prevent sugar export out of the leaf or by exogenously feeding sugar to algae or cell cultures.…”

“…1 for a schematic representation of the interactions discussed here). Long-term growth at elevated CO 2 , for example, generally increases soluble sugar concentration in leaves (Van Oosten and Besford, 1994;Cheng et al, 1998). Such leaves often have lower Rubisco transcript levels and decreased photosynthetic capacity (Krapp et al, 1993;Besford, 1994, 1995;Cheng et al, 1998).…”