JXB Advance Access originally published online on July 1, 2003
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Journal of Experimental Botany, Vol. 54, No. 389, pp. 1969-1975,
August 1, 2003
© 2003 Oxford University Press
Development of C4 photosynthesis in sorghum leaves grown under free-air CO2 enrichment (FACE)
Received 12 April 2003; Accepted 22 April 2003
1 Department of Plant Biology and Center for the Study of Early Events in Photosynthesis, Arizona Sate University, PO Box 871601, Tempe, AZ 85287–1601, USA
2 USDA, Agricultural Research Service, US Water Conservation Laboratory, Phoenix, AZ 85040, USA
3 Department of Plant Science, University of Arizona, Tucson, AZ 85721, USA
4 Laboratory of Tree Ring Research, University of Arizona, Tucson, AZ 85721, USA
* To whom correspondence should be addressed. Fax: +1 480 965 6899. E-mail: andrew.webber{at}asu.edu
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Abstract |
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The developmental pattern of C4 expression has been well characterized in maize and other C4 plants. However, few reports have explored the possibility that the development of this pathway may be sensitive to changes in atmospheric CO2 concentrations. Therefore, both the structural and biochemical development of leaf tissue in the fifth leaf of Sorghum bicolor plants grown at elevated CO2 have been characterized. Ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and phosphoenolpyruvate carboxylase (PEPC) activities accumulate rapidly as the leaf tissue differentiates and emerges from the surrounding whorl. Rubisco was not expressed in a cell-specific manner in the youngest tissue at the base of the leaf, but did accumulate before PEPC was detected. This suggests that the youngest leaf tissue utilizes a C3-like pathway for carbon fixation. However, this tissue was in a region of the leaf receiving very low light and so significant rates of photosynthesis were not likely. Older leaf tissue that had emerged from the surrounding whorl into full sunlight showed the normal C4 syndrome. Elevated CO2 had no effect on the cell-specific localization of Rubisco or PEPC at any stage of leaf development, and the relative ratios of Rubisco to PEPC remained constant during leaf development. However, in the oldest tissue at the tip of the leaf, the total activities of Rubisco and PEPC were decreased under elevated CO2 implying that C4 photosynthetic tissue may acclimate to growth under elevated CO2.
Key words: C4 expression, elevated CO2, leaf tissue. Sorghum bicolor, structural and biochemical development.
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Introduction |
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The ability of C4 plants to elevate the levels of CO2 around ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) in the bundle sheath cells (BSC) limits the rate of photorespiration and its associated loss of energy, as well as allowing Rubisco to function at nearly its maximum rate of catalysis (Edwards and Walker, 1983). Based on this it is generally assumed that C4 plants will not respond to growth under elevated atmospheric [CO2] concentrations. However, a number of studies have shown enhanced photosynthesis and/or growth of C4 plants under elevated atmospheric [CO2] (Poorter et al., 1996; Wand et al., 1999; Cousins et al., 2001; Ottman et al., 2001; Wall et al., 2001). Typically, the increased growth response to elevated atmospheric [CO2] of C4 plants is attributed to the indirect CO2 effect of stomatal closure and subsequent increased water use efficiency (WUE) and water potential (Ziska et al., 1999; Wall et al., 2001). However, it has also been shown that C4 species respond directly to increased atmospheric [CO2] independent of any improvement in leaf water potential (Ghannoum et al., 1997; Maroco et al., 1999; Ziska et al., 1999; Cousins et al., 2001).
Recent studies indicate that growth of C4 plants under elevated atmospheric [CO2] may lead to acclimation of certain photosynthetic enzymes. For example, Rubisco, but not phosphoenolpyruvate carboxylase (PEPC), activity was reduced in mature maize plants grown under 3-fold ambient levels of atmospheric [CO2] (Maroco et al., 1999). In another growth chamber experiment, the total amount of PEPC, but not Rubisco, was reduced in the mature leaves of sorghum plants grown under double atmospheric [CO2] (Watling et al., 2000). Although the developmental pattern of C4 expression has been well characterized in maize and other C4 leaves, the possibility that the development of the C4 pathway may be sensitive to changes in growth atmospheric [CO2] has not been addressed.
In graminaceous plants, leaf cells divide from a basal meristem, which causes older cells to be displaced by younger cells below them (Nelson and Langdale, 1989). This type of developmental pattern creates a positional gradient of cell ages; with younger, less differentiated cells near the base and older, more differentiated cells toward the tip (Martineau and Taylor, 1985). It has been well documented in maize, a NADP-type C4 plant closely related to sorghum, that as young leaf tissues differentiate from the leaf primordia they switch from a C3-type protein expression to an expression characteristic of C4 photosynthesis (Nelson and Dengler, 1992; Langdale et al., 1988a, b, 1989a, b).
The development and expression of C4 photosynthetic genes shows a temporal and spatial pattern that mirrors the developmental and age gradients of the leaf cells (Sheen, 1999). Additionally, light signals enhance C4 gene expression in the BSC (e.g. NADP-malate dehydrogenase and Rubisco) as well as suppress expression of Rubisco in the mesophyll cells. It has also been shown that C4 gene expression is regulated by signals derived from a diverse set of abiotic factors. For example, nitrogen starvation induces the accumulation of transcripts encoding PEPC and other C4 genes by both transcriptional and post-transcriptional mechanisms (Sakakibara et al., 1998; Sugiyama, 1998). Additionally, the amphibious sedge E. vivipara develops Kranz anatomy and uses C4 photosynthesis under terrestrial conditions but switches back to C3 photosynthesis and anatomy when submerged under water (Ueno, 1996). Taken together, these observations imply that the expression and regulation of C4 photosynthesis is a dynamic process, which may help C4 plants cope with changing environmental conditions and carbon metabolism requirements.
These observations also raise the intriguing possibility that development of the C4 pathway may be sensitive to elevated atmospheric [CO2]. It is possible that enhanced productivity of C4 crops is in part due to the fact that younger leaves are more C3-like and are thus more sensitive to elevated CO2. Indeed, it has previously been observed that C4 photosynthesis in young fully expanded Sorghum bicolor leaves was more responsive then older leaves to growth under elevated atmospheric [CO2] in a free-air CO2 enrichment (FACE) experiment (Cousins et al., 2001). If elevated atmospheric [CO2] delayed the development of the C4 pathway, this delay may further increase the sensitivity of C4 crops to elevated atmospheric [CO2].
The goals of this research are (1) to characterize the development of the C4 pathway in sorghum leaves; (2) to assess whether or not growth under elevated atmospheric CO2 concentrations would alter the development and cell specific expression of key C3 and C4 enzymes; and (3) to determine if the photosynthetic enzyme activity is affected by growth under elevated atmospheric [CO2]. To test these questions, a Sorghum bicolor crop was grown in the field under a free-air CO2 enrichment (FACE) experiment at control (370 ppm) and FACE (570 ppm) atmospheric CO2 concentrations. the anatomical development, tissue specific compartmentalization and activity of obligatory enzymes involved in C4 photosynthesis grown under FACE and control conditions have been characterized.
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Materials and methods |
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FACE methodology
Free-air CO2 enrichment (FACE) experiments were conducted at the University of Arizona, Maricopa Agricultural Center (MAC), Maricopa, AZ, USA in 1998 to determine the interactive effects of elevated CO2 and drought on Sorghum bicolor (L.) Moench (see Ottman et al., 2001, for a comprehensive description of the sorghum FACE experiment).
CO2 treatments
The free-air CO2 enrichment (FACE) technique was used to enrich the air in circular plots within a sorghum field in a similar way to earlier experiments (Hendrey et al., 1993; Wechsung et al., 1995; Hunsaker et al., 1996; Kimball et al., 1999). Briefly, four replicate 25 m diameter toroidal plenum rings constructed from 0.305 m diameter pipe were placed in the field shortly after planting. The mean daytime values were 566 µl l–1 and 373 µl l–1 and the mean night-time values were 607 µl l–1 and 433 µl l–1 for FACE and control, respectively.
Crop culture
Certified grain sorghum seed (Dekalb DK54), which had been treated with fungicide (Captan, Chloropyrifos-methyl, Fluxofenium, and Metalaxyl), was planted into relatively dry soil in north–south rows spaced 0.76 m (30 inches) apart at a rate of 318 000 seeds ha–1. Immediately after planting, erection of the FACE and control apparatus commenced and was completed when the first irrigation was applied to all plots.
Leaf sampling
Two weeks after the initial irrigation, leaf tissue was sampled prior to the initiation of the ligule on the fifth leaf to emerge after the coeloptile on 8 August 1998. Six randomly chosen plants from each CO2 treatment were harvested. The lengths of the fifth and sixth leaves were measured from the base of the plant to the tip of each leaf respectively. The coeloptile and all prior sheaths surrounding the fifth leaf were removed down to the seed. The fifth leaf was subsequently sectioned into five portions as illustrated in Fig. 1 and the area of leaf tissue for each section was determined with a CI-202 leaf area meter (CID, Inc. Vancouver, WA USA). Leaf tissue sections from three of the six leaves were immediately stored in liquid nitrogen in prelabelled vials for future biochemical analysis as previously described. The remaining leaf sections were fixed in a FAA fixative (2% formaldehyde, 50% ethanol and 5% glacial acetic acid) overnight at room temperature (Robertson and Leech, 1995).
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Immunolocalization
Leaf sections were dehydrated in water to ethanol dilution series followed by an ethanol to tert-butanol (2-methyl-2-propanol) dilution series. Sections were then infiltrated in a tert-butanol to paraplast-plus dilution series before being washed and embedded in 100% paraplast-plus (Oxford Labware, St Louis MO). Transverse sections (10 µm) were cut using a Spencer No. 820 rotary microtome (American Optical Company, Buffalo, NY, USA) and adhered to a poly-lysine coated slide. Sections were then dewaxed in 100% xylenes and rehydrated in an ethanol to water series. Subsequently, the slides were placed in a phosphate buffer PBS (0.16 M NaCl, 8.0 mM Na2HPO4, 2.7 mM KCl, and 1.5 mM KH2PO4) for 15 min then incubated at 4 °C overnight with the polyclonal primary rabbit anti-Rubisco and rabbit anti-PEPC (1:2000) in 0.5% BSA in PBS. Sections were then washed and incubated with fluorescein isothiocyanate (FITC) conjugated secondary IGg antibodies (1:3000) for 1 h (Jackson-immuno, West Grove, PA USA). Protein compartmentalization was then visualized on a Leica DM RBE microscope equipped with a Leica TCS NT confocal scanning head equipped with the manufacturer’s filters set-up for FITC dyes and an argon laser (488 nm) (Leica, Heidelberg, Germany). Images were composed and analysed using Adobe PhotoShop 5.0.
Biochemical assays
Leaf tissue was removed from liquid nitrogen and ground in an ice-cold glass homogenizer containing 100 mM Tricine (pH 8), 10 mM MgCl2, 1 mM EDTA, 14 mM DTT, 2% PVP, 20% glycerol, 1 mM PMSF, and 1 mM NaFl at a ratio of 1 cm2 leaf tissue to 1 ml buffer. Aliquots were assayed for maximum activity of Rubisco using a 100 mM Tricine (pH 8) buffer containing 10 mM MgCl2, 2 mM DTT, 10 mM 14C-labelled sodium bicarbonate, and 0.4 mM RuBP. For Rubisco maximum activity, the leaf homogenate was allowed to incubate with sodium bicarbonate for 10 min before the assay. Additional aliquots were assayed for PEPCase activity using 50 mM Hepes-KOH, 5 mM MgCl2, 10 mM 14C-labelled sodium bicarbonate, 10 U ml–1 MDH, and 0.2 mM NADH under optimal conditions (pH 8 and 5 mM PEP). Each reaction was timed for 30 s and then terminated with HCl/HCOOH (1 N/4 N). After centrifugation, total soluble protein was measured using Coomassie Plus reagent (Pierce) according to manufactures methodology.
Statistical analysis
The enzyme activity data were analysed using PROC MIXED for the analysis of variance in SAS (SAS Institute, Cary, NC, USA). Leaf section was considered a repeated factor for the enzyme activity data and post hoc pairwise comparisons were made using Tukey’s probability.
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Results |
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Leaf growth
There was no difference in the length of the fifth or sixth leaves due to growth under elevated atmospheric [CO2] (Fig. 2a, b). In addition, the total leaf area of the fifth leaf did not differ between treatments (Fig. 2c). The individual sections (1–5) of leaf 5 differed in total area only slightly in section 1 which is the youngest leaf tissue just above the apical meristem (Fig. 2d).
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Regardless of CO2 treatment, the total extractable protein in the young developing leaves was highest in section 1 compared to the remaining sections (Fig. 3a). In the older leaf sections the protein levels remained relatively constant (1 g protein m–2 of leaf tissue). Growth CO2 conditions had no effect on the total protein content in any of the leaf sections. Total chlorophyll per leaf area (chl m–2) increased steadily from sections 1 to 5 as the fifth leaf emerged from the surrounding whorl (Fig. 3b). There was, however, no treatment effect on the total amounts of chlorophyll in any section of leaf.
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Enzyme activities
Enzyme activities expressed on a total extractable protein basis (µmol CO2 mg–1 protein) or on a total chlorophyll content (µmol CO2 mg–1 chlorophyll) increased steadily as the leaf tissue differentiated and emerged from the surrounding whorl (Fig. 4a, b). CO2 treatment, however, had no effect on either Rubisco or PEPC activities when assayed on a per protein or a per chlorophyll basis (not shown). However, on a leaf area basis, Rubisco and PEPC activity (µmol CO2 m–2 s–1) was higher depending on the leaf section in the control plots as compared to the FACE plots (Fig. 4c, d; F=4.11; P <0.05 and F=5.51; P <0.01, respectively). Rubisco and PEPC activities were significantly higher in control plants only in sections 4 and 5 as determined by Tukey’s pairwise comparison (P <0.05; P <0.01 and P <0.01; P <0.01, respectively). The ratio of PEPC to Rubisco total activity remained relatively constant during leaf development and was not affected by growth under elevated atmospheric [CO2].
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Development of Kranz anatomy and enzyme localization
Under both CO2 growth conditions the Kranz anatomy appeared fully developed and the chloroplasts within the bundle sheath cells were large and centrifugally arranged in the third section prior to the emergence of the leaf tissue from the surrounding whorls (Fig. 5). In the younger tissues (leaf sections 1 and 2) a definitive Kranz anatomy was not apparent and the chloroplast in both the mesophyll cells and the BSC were small and arranged primarily adjacent to all faces of the cell walls (Fig. 5a–b, f–g). PEPC was undetectable via immunolabelling in the earliest leaf tissue (sections 1 and 2). However, in older leaf tissue (sections 3–5) PEPC occurred only in the cytosol of the mesophyll cells under both growth treatments (Fig. 5f–j). Rubisco localized exclusively to the chloroplast of the bundle sheath cells in sections 3–5 and appeared to be BSC localized even in the second leaf section (Fig. 5b–e). In the very young leaf tissue (section 1) Rubisco localized in the chloroplast of both the mesophyll cells and BSC (Fig. 5a). The differential tissue expression of Rubisco was unaffected by either growth CO2 condition.
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Discussion
In order to determine the effect of elevated atmospheric [CO2] on the growth and development of the C4 pathway, both the structural and biochemical development of leaf tissue in the fifth leaf of Sorghum bicolor have been characterized. the appearance, accumulation and cell specific expression of key C4 pathway enzymes during the development of this particular leaf were measured directly. Extremely large changes in leaf tissue anatomy and biochemistry occurred in a very short period of development. In the youngest leaf tissue the chloroplasts were small and randomly arranged against the cell wall. The total enzyme activities of Rubisco and PEPC were low and virtually undetectable by immunolocalization (Figs 4, 5). Similar to what would be expected for a C3 plant, Rubisco was located in both the mesophyll and BSC chloroplast in the youngest leaf tissue (Fig. 5a). By contrast with mature C4 leaf tissue, PEPC immunolocalization was undetectable in these same young leaf tissues (Fig. 5f). These observations are consistent with previous work on developing maize leaves where Rubisco appears significantly before PEPC accumulates (Nelson et al., 1984). The BSC chloroplasts in the second leaf section were not enlarged nor centrifugally arranged, as typically seen in mature leaf tissue. However, Rubisco immunolocalized exclusively to the BSC chloroplast (Fig. 5b). These observations are again consistent with earlier work in developing maize leaves, which showed that mRNA for the large and small subunits of Rubisco accumulate exclusively in the BSC chloroplast before the cells are fully differentiated (Martineau and Taylor, 1985). PEPC expression was still undetectable in the second leaf section (Fig. 5g). By the third leaf section the BSC chloroplasts were enlarged, centrifugally arranged and contained large amounts of Rubisco (Fig. 5c), and PEPC occurred only in the cytosol of the mesophyll cells (Fig. 5h). Both Rubisco and PEPC activity accumulated very rapidly as the leaf tissue differentiated further and emerged from the surrounding whorl (Fig. 4). The total amount of leaf protein per unit area remained relatively constant after the first leaf section. However, total chloroplast and total enzyme activities of Rubisco and PEPC continued to increase as the leaf developed and emerged from the whorl.
From these observations it appears that Rubisco is not expressed in a cell-specific manner in very young leaf tissue. In addition, Rubisco accumulates before significant amounts of PEPC are detectable. Thus, the cells at very early stages of leaf development must utilize a C3-like pathway for carbon fixation. Although this young leaf tissue may in fact have C3-like characteristics, the cells are under very low light conditions inside the whorls and significant rates of photosynthesis are unlikely. By the time the leaf tissue emerges from the surrounding whorl and into full sunlight, the C4 apparatus appears to be fully expressed.
By contrast to C3 plants, elevated CO2-induced photosynthetic acclimation is not commonly observed in C4 plants. In C3 plants acclimation to long-term exposure to elevated CO2 usually causes a decrease in the photosynthetic capacity associated with reduced levels of Rubisco and other C3 cycle enzymes (Stitt, 1991; Sage, 1994; Webber et al., 1994; Nie et al., 1995; Ghannoum et al., 2000). In C4 plants elevated CO2 may allow alterations in the content or activity of some C3 and C4 cycle enzymes without losses in the rates of CO2 assimilation (Maroco et al., 1999). In this experiment the relative ratios of Rubisco to PEPC remained constant during leaf development. However, the total activities of Rubisco and PEPC decreased under elevated CO2 implying that young C4 photosynthetic plant tissue may acclimate to growth under elevated CO2. These data are consistent with the results of previously published work, which showed that photosynthesis in the upper most fully expanded fifth leaf was consistently lower in response to changes in intercellular CO2 in FACE-grown plants as compared to control plants (Cousins et al., 2001; see Fig. 2e, f). Although these gas exchange data were collected during the second year of the FACE sorghum experiment, it further substantiates enzymatic data indicating that C4 photosynthesis may acclimate to growth under elevated CO2.
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Conclusions |
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Although young sorghum leaf tissues express C3-like photosynthetic characteristics, it seems unlikely that rates of photosynthesis are significant in these cells. By the time cells emerge from the surrounding whorl and into full sunlight, the mesophyll and BSC are nearly fully differentiated. In the older leaf tissue, PEPC and Rubisco activities have increased significantly and appear to be localized in a cell-specific manner. In this same leaf tissue the total enzyme activities of PEPC and Rubisco are lower under elevated CO2 compared with control plants. This apparent acclimation response is possibly attributable to the increased capacity for carbon fixation and the efficiency with which the C4-pump is able to concentrate CO2 within the BSC under CO2 enrichment
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Acknowledgements |
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Asaph Cousins acknowledges support from a NSF Graduate Research Training Grant (DGE-9553456). The research was supported by Interagency Agreement No DE-AI03-97ER62461 between the Department of Energy, Office of Biological and Environmental Research, Environmental Sciences Division and the USDA, Agricultural Research Service BAK); by Grant No. 97-35109-5065 from the USDA, Competitive Grants Program to the University of Arizona (SWL); and by the USDA, Agricultural Research Service as part of the DOE/NSF/NASA/USDA/EPA Joint Program on Terrestrial Ecology and Global Change (TECO III). The research was also supported by Interagency Agreement No. IBN-9652614 between the National Science Foundation and the USDA, Agricultural Research Service (Gerard W Wall, PI) as part of the NSF/DOE/NASA/USDA Joint Program on Terrestrial Ecology and Global Change (TECO II); and, by the USDA, Agricultural Research Service. This work contributes to the Global Change Terrestrial Ecosystem (GCTE) Core Research Programme, which is part of the International Geosphere–Biosphere Programme (IGBP). Confocal imaging was conducted in the WM Keck BioImaging Laboratory at Arizona State University. Antisera were provided by Dr M Salvucci (PEPC) and Dr W Frasch (Rubisco). We also acknowledge the helpful co-operation of Dr Robert Roth and his staff at the Maricopa Agricultural Center. Portions of the FACE apparatus were furnished by Brookhaven National Laboratory, and we are grateful to Mr Keith Lewin, Dr John Nagy, and Dr George Hendrey for assisting in its installation and consulting about its use.
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References |
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|---|
Cousins AB, Adam NR, Wall GW, et al. 2001. Reduced photorespiration and increased energy-use efficiency in young CO2-enriched sorghum leaves. New Phytologist 150, 275–284.[CrossRef][Web of Science]
Edwards GE, Walker DA. 1983. C3, C4: mechanisms and cellular and environmental regulation of photosynthesis. Los Angeles, CA: University of California Press.
Ghannoum O, von Caemmerer S, Barlow EWR, Conroy JP. 1997. The effects of CO2 enrichment and irradiance on the growth, morphology and gas exchange of a C3 (Panicum laxum) and a C4 (Panicum antidotale) grass. Australian Journal of Plant Physiology 24, 227–237.[Web of Science]
Ghannoum O, von Caemmerer S, Ziska LH, Conroy JP. 2000. The growth response of C4 plants to rising atmospheric CO2 partial pressure: a reassessment. Plant, Cell and Environment 23, 931–942.[CrossRef]
Hendrey G, Lewin K, Nagy J. 1993. Control of carbon dioxide in unconfined field plots. In: Schulze ED, Mooney HA, eds. Design and execution of experiments on CO2 enrichment. Environmental Research Programme, Ecosystems Research Report Series, Report No. 6. Brussels: Commission of the European Communities, 309–327.
Hunsaker DJ, Kimball BA, Pinter Jr PJ, LaMorte RL, Wall GW. 1996. CO2 enrichment and irrigation effects on wheat evapotranspiration in a free-air environment. Transactions of the American Society of Agricultural Engineers 39, 1345–1355.
Kimball BA, LaMorte RL, Pinter Jr PJ, Wall GW, Hunsaker DJ, Adamsen FJ, Leavitt SW, Thompson TL, Matthias AD, Brooks TJ. 1999. Free-air CO2 enrichment (FACE) and soil nitrogen effects on energy balance and evapotranspiration of wheat. Water Resources Research 35, 1179–1190.[CrossRef]
Langdale JA, Lane B, Freeling M, Nelson T. 1989b. Cell lineage analysis of maize bundle sheath and mesophyll cells. Developmental Biology 133, 128–139.[CrossRef][Web of Science][Medline]
Langdale JA, Rothermel BA, Nelson T. 1988a. Cellular pattern of photosynthetic gene expression in developing maize leaves. Genes and Development 2, 106–115.
Langdale JA, Rothermel BA, Nelson T. 1989a. Cellular pattern of photosynthetic gene expression in developing maize leaves. Genes and Development 2, 106–115.
Langdale JA, Zelitch I, Miller E, Nelson T. 1988b. Cell position and light influence C4 versus C3 patterns of photosynthetic gene expression in maize. EMBO Journal 7, 3643–3651.[Web of Science][Medline]
Maroco JP, Edwards GE, Ku MSB. 1999. Photosynthetic acclimation of maize to growth under elevated levels of carbon dioxide. Planta 210, 115–125.[CrossRef][Web of Science][Medline]
Martineau B, Taylor WC. 1985. Photosynthetic gene expression and cellular differentiation in developing maize leaves. Plant Physiology 78, 399–404.
Nelson T, Dengler NG. 1992. Photosynthetic tissue differentiation in C4 plants. International Journal of Plant Science 153, S105.
Nelson T, Harpster MH, Mayfield SP, Taylor WC. 1984. Light-regulated gene expression during maize leaf development. Journal of Cell Biology 98, 558–564.
Nelson T, Langdale JA. 1989. Patterns of leaf development in C4 plants. The Plant Cell 1, 3–13.[Medline]
Nie GY, Long SP, Garcia RL, Kimball BA, LaMorte RL, Pinter Jr PJ, Wall GW, Webber AN. 1995. Effects of free-air CO2 enrichment on the development of the photosynthetic apparatus in wheat, as indicated by changes in leaf protein. Plant, Cell and Environment 18, 855–864.
Ottman MJ, Kimball BA, Pinter Jr PJ, Wall GW, Vanderlip RL, Leavitt SW, LaMorte RL, Matthias AD, Brooks TJ. 2001. Elevated CO2 increases sorghum biomass under drought conditions. New Phytologist 150, 261–273.[CrossRef][Web of Science]
Poorter H, Roumet C, Campbell BD. 1996. Interspecific variation in the growth response of plants to elevated CO2: a search for functional types. In: Korner C, Bazzaz FA, eds. Carbon dioxide, populations, and communities. New York, USA: Academic Press, 375–412.
Robertson EJ, Leech RM. 1995. Significant changes in cell and chloroplast development in young wheat leaves (Triticum aestivum cv. Hereward) grown in elevated CO2. Plant Physiology 107, 63–71.[Abstract]
Sage RF. 1994. Acclimation of photosynthesis to increasing atmospheric CO2: the gas exchange perspective. Photosynthesis Research 39, 351–368.
Sakakibara H, Suzuki M, Takei K, Deji A, Taniguchi M, Sugiyama T. 1998. A response-regulator homolgue possibly involved in nitrogen signal transduction mediated by cytokinin in maize. The Plant Journal 14, 337–44.[CrossRef][Web of Science][Medline]
Sheen J. 1999. C4 gene expression. Annual Review of Plant Physiology and Plant Molecular Biology 50, 187–217.[CrossRef][Web of Science][Medline]
Stitt M. 1991. Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells. Plant, Cell and Environment 14, 741–762.
Sugiyama T. 1998. Nitrogen-responsive expression of C4 photosynthesis genes in maize. In: Satoh K, Murata N, eds. Stress responses of photosynthetic organisms. Tokyo, Japan: Elsevier Press, 167–180.
Ueno O. 1996. Structural characterization of photosynthetic cells in an amphibious sedge, Eleocharis vivipara, in relation to C3 and C4 metabolism. Planta 199, 382–393.
Wall GW, Brooks TJ, Adam NR, et al. 2001. Elevated atmospheric CO2 improved sorghum plant water status by ameliorating the adverse effects of drought. New Phytologist 152, 438–473.
Wand SJE, Midgley GF, Jones MH, Curtis PS. 1999. Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentration: a test of current theories and perceptions. Global Change Biology 5, 723–741.[CrossRef]
Watling JR, Press MS, Quick WP. 2000. Elevated CO2 induces biochemical and ultrastructural changes in leaves of C4 cereal sorghum. Plant Physiology 123, 1143–1152.
Webber AN, Long SP, Nie G-Y. 1994. Acclimation of photosynthetic proteins to rising atmospheric CO2. Photosynthesis Research 39, 413–425.
Wechsung G, Wechsung F, Wall GW, Adamsen F, Kimball BA, Garcia RL, Pinter Jr PJ, Kartschall T. 1995. Biomass and growth rate of a spring wheat root system grown in free-air CO2 enrichment (FACE) and ample moisture. Journal of Biogeography 22, 623–634.[CrossRef]
Ziska LH, Sicher RC, Bunce JA. 1999. The impact of elevated carbon dioxide on the growth and gas exchange of three C4 species differing in CO2 leak rates. Physiologia Plantarum 105, 74–80.
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