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RESEARCH ARTICLE
Contents Vol 36(9)

Enhancement in leaf photosynthesis and upregulation of Rubisco in the C4 sorghum plant at elevated growth carbon dioxide and temperature occur at early stages of leaf ontogeny

P. V. Vara Prasad A D , Joseph C. V. Vu B , Kenneth J. Boote C and L. Hartwell Allen Jr B
+ Author Affiliations
- Author Affiliations

A Agronomy Department, 2004 Throckmorton Hall, Kansas State University, Manhattan, KS 66506, USA.

B United States Department of Agriculture – Agricultural Research Service, Center for Medical, Agricultural and Veterinary Entomology, Chemistry Research Unit, Gainesville, FL 32608, USA.

C Agronomy Department, 304 Newell Hall, University of Florida, Gainesville, FL 32611, USA.

D Corresponding author. Email: vara@ksu.edu

Functional Plant Biology 36(9) 761-769 https://doi.org/10.1071/FP09043
Submitted: 21 February 2009  Accepted: 21 July 2009   Published: 3 September 2009

Abstract

Rising atmospheric carbon dioxide (CO2) concentration and temperature will influence photosynthesis, growth and yield of agronomic crops. To investigate effects of elevated CO2 and high temperature on leaf gas exchanges, activities of Rubisco and phosphoenolpyruvate carboxylase (PEPC) and growth of grain sorghum (Sorghum bicolor L. Moench), plants were grown in controlled environments at day-time maximum/night-time minimum temperatures of 30/20°C or 36/26°C at ambient (350 µmol mol–1) or elevated (700 µmol mol–1) CO2. Gas-exchange rates, activities of Rubisco and PEPC and growth parameters (leaf, stem and total dry weights) were determined at different stages of leaf development. Between 6 and 25 days after leaf tip emergence, leaf carbon exchange rate (CER) of elevated CO2 plants was greater at 30/20°C and 36/26°C than that of ambient CO2 plants at the same temperatures. The positive response of CER to elevated CO2 was greater in young leaves than in old leaves. In young leaves, elevated CO2 enhanced Rubisco activity at 30/20°C and 36/26°C, whereas PEPC activity was not affected by elevated CO2 at 30/20°C but was marginally enhanced at 36/26°C. At 30/20°C, growth parameters were not affected by elevated CO2 until 50 days after sowing (DAS); at 36/26°C, they were progressively enhanced by elevated CO2 to as high as 49 to 62% by 50 DAS. Leaf CER and Rubisco activity were enhanced by elevated CO2 at early stages of leaf ontogeny for the C4 grain sorghum. Such enhancement should have a significant role in dry matter production under elevated CO2.

Additional keywords: climate change, dry matter production, heat stress, leaf development, leaf growth, Sorghum bicolor.


Acknowledgements

This research was supported by the Florida Agricultural Experiment Station of the University of Florida and the US Department of Agriculture-Agricultural Research Service and Kansas Agricultural Experiment Station. Our sincere thanks to Joan Anderson for her excellent help throughout the experiment and in conducting the enzyme assays. We thank Larry Pitts, Wayne Wynn and Maritza Romero for engineering support; Drs Prem Chourey, Mukesh Jain and Jean Thomas for their scientific support, and Dr Richard Vanderlip for supplying the sorghum seeds. This is contribution No. 09–247-J from the Kansas Agricultural Experiment Station.


References


Allen LH, Pan D, Boote KJ, Pickering NB, Jones JW (2003) Carbon dioxide and temperature effects of evapotranspiration and water-use efficiency of soybean. Agronomy Journal 95, 1071–1081. open url image1

Ashton AR , Burnell JN , Furbank RT , Jenkins CLD , Hatch MD (1990) Enzymes of C4 photosynthesis. In ‘Methods in Plant Biochemistry, Volume 3’. (Ed. PJ Lea) pp. 39–72. (Academic Press: San Diego, CA)

Berry JA, Bjorkman O (1980) Photosynthetic response and adaptation to high temperature stress in plants. Annual Review of Plant Physiology 31, 491–543.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Bowes G (1993) Facing the inevitable: plants and increasing atmospheric CO2. Annual Review of Plant Physiology and Plant Molecular Biology 44, 309–332.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Catsky J , Sestak Z (1997) Photosynthesis during leaf development. In ‘Handbook of photosynthesis’. (Ed. M Pessarakli) pp. 633–660. (Marcel Dekker: New York)

Cousins AB, Adam NR, Wall GW, Kimball BA, Pinter PJ , et al . (2001) Reduced photorespiration and increased energy-use efficiency in young CO2-enriched sorghum leaves. New Phytologist 150, 275–284.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Cousins AB, Adam NR, Wall GW, Kimball BA, Pinter PJ, Ottman MJ, Leavitt SW, Webber AN (2003) Development of C4 photosynthesis in sorghum leaves grown under free-air CO2 enrichment (FACE). Journal of Experimental Botany 54, 1969–1975.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Crafts-Brandner SJ, Salvucci ME (2002) Sensitivity of photosynthesis in a C4 plant, maize, to heat stress. Plant Physiology 129, 1773–1780.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Drake BG, Gonzales-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Annual Review of Plant Physiology and Plant Molecular Biology 48, 609–639.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dwyer SA, Ghannoum O, Nicotra A, von Caemmerer S (2007) High temperature acclimation of C4 photosynthesis is linked to changes in photosynthetic biochemistry. Plant, Cell & Environment 30, 53–66.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Furbank R, Hatch MD (1987) Mechanism of C4 photosynthesis: the size and composition of the inorganic carbon pool in bundle sheath cells. Plant Physiology 85, 958–964.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Geiger M, Haake V, Ludewig F, Sonnewald U, Sitt M (1999) 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. Plant, Cell & Environment 22, 1177–1199.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Ghannoum O, von Caemmerer S, Barlow EWR, Conroy JP (1997) The effect 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. open url image1

Ghannoum O, Siebke K, von Caemmerer S, Conroy JP (1998) The photosynthesis of young Panicum C4 leaves is not C3-like. Plant, Cell & Environment 21, 1123–1131.
| Crossref | GoogleScholarGoogle Scholar | open url image1

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 & Environment 23, 931–942.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Hatch MD (1987) C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochimica et Biophysica Acta 895, 81–106. open url image1

He D, Edwards GE (1996) Estimation of diffusion resistance of bundle sheath cells to CO2 from modeling of C4 photosynthesis. Photosynthesis Research 49, 195–208.
| Crossref | GoogleScholarGoogle Scholar | open url image1

IPCC Intergovernmental Panel on Climate Change (2007) ‘Fourth assessment report. Synthesis report.’ (World Meteorological Organization: Geneva)

Law RD, Crafts-Brandner SJ (1999) Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiology 120, 173–182.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Leakey ADB, Uribelarrea M, Ainsworth EA, Naidu SL, Rogers A, Ort DR, Long SP (2006) Photosynthesis, productivity, and yield of maize are not affected by open-air elevation of CO2 concentration in the absence of drought. Plant Physiology 140, 779–790.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lilley RM, Walker DA (1974) An improved spectrophotometric assay for ribulose-bisphosphate carboxylase. Biochimica et Biophysica Acta 358, 226–229.
| PubMed |
open url image1

Long SP (1999) The biology of C4 photosynthesis: environmental responses. In ‘The biology of C4 photosynthesis’. (Eds RF Sage, PK Monson) pp. 21–249. (Academic Press: San Diego, FL)

Matsuoka M, Furbank RT, Fukayama H, Miyao M (2001) Molecular engineering of C4 photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 52, 297–314.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Morison JIL, Lawlor DW (1999) Interaction between increasing CO2 concentration and temperature on plant growth. Plant, Cell & Environment 22, 659–682.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Nelson T, Langdale JA (1992) Developmental genetics of C4 photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 43, 25–47.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Ogren WL (1984) Photorespiration; pathways, regulation, and modification. Annual Review of Plant Physiology and Plant Molecular Biology 35, 415–442.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Osborne CP, LaRoche J, Garcia RL, Kimball BA, Wall GW, Pinter PJ, LaMorte RL, Hendrey GR, Long SP (1998) Does leaf position within a canopy affect acclimation of photosynthesis to elevated CO2? Analysis of a wheat crop under free-air CO2 enrichment. Plant Physiology 117, 1037–1045.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Parton WJ, Logan JA (1981) A model for diurnal variation in soil and air temperature. Agricultural Meteorology 23, 205–216.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Pittermann J, Sage RF (2001) The response of the high altitude C4 grass Muhlenbergia montanum (Nutt.) A.S. Hitchc. to long- and short-term chilling. Journal of Experimental Botany 52, 829–838.
| PubMed |
open url image1

Poorter H , Roumer C , Campbell BD (1996) Interspecific variation in the growth response of plant to elevated CO2: a search for functional types. In ‘Carbon dioxide, populations and communities’. (Eds C Korner, FA Bazzaz) pp. 375–412. (Academic Press: New York)

Prasad PVV, Boote KJ, Allen LH, Thomas JMG (2002) Effects of elevated temperature and carbon dioxide on seed-set and yield of kidney bean (Phaseolus vulgaris L.). Global Change Biology 8, 710–721.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Prasad PVV, Boote KJ, Allen LH, Thomas JMG (2003) Supra-optimal temperatures are detrimental to peanut (Arachis hypogaea L.) reproductive processes and yield at ambient and elevated carbon dioxide. Global Change Biology 9, 1775–1787.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Prasad PVV, Boote KJ, Allen LH (2006) Adverse of high temperature effects on pollen viability, seed-set, seed yield and harvest index of grain-sorghum [Sorghum bicolor (L). Moench] are more severe at elevated carbon dioxide due to higher tissue temperatures. Agricultural and Forest Meteorology 139, 237–251.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Roger HH, Bingham GE, Cure JD, Smith JM, Surano KA (1983) Responses of selected plant species to elevated carbon dioxide in the field. Journal of Environmental Quality 12, 569–574. open url image1

Sage RF, Sharkey TD, Pearcy RW (1990) The effect of leaf nitrogen and temperature on the CO2 response of photosynthesis in Chenopodium album L., a C3 dicot. Australian Journal of Plant Physiology 17, 135–148. open url image1

Sage RF, Santrucek J, Grise DJ (1995) Temperature effects on the photosynthetic response of C3 plants to long-term CO2 enrichment. Vegetatio 121, 67–77.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Sharkey TD, Savitch LV, Butz ND (1991) Photometric method for routine determination of K cat and carbamylation of rubisco. Photosynthesis Research 28, 41–48.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Siebke K, Ghannoum O, Conroy JP, von Caemmerer S (2002) Elevated CO2 increases leaf temperature of two glasshouse-grown C4 grasses. Functional Plant Biology 29, 1377–1385.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Vu JCV, Allen LH, Boote KJ, Bowes G (1997) Effects of elevated CO2 and temperature on photosynthesis and Rubisco in rice and soybean. Plant, Cell & Environment 20, 68–76.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Vu JCV , Allen LH Jr , Gallo-Meagher M (2002) Crop plant responses to rising CO2 and climate change. In ‘Handbook of plant and crop physiology’. (Ed. M Pessarakli) pp. 35–55. (Marcel Dekker: New York)

Wand SJE, Midgley GE, Jones MH, Curtis PS (1999) Response 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 | GoogleScholarGoogle Scholar | open url image1

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. Plant Physiology 105, 74–80.
| Crossref | GoogleScholarGoogle Scholar | open url image1