The Effects of Elevated CO2 Concentration on Soybean Gene Expression. An Analysis of Growing and Mature Leaves1[W][OA]

Improvements in carbon assimilation and water-use efficiency lead to increases in maximum leaf area index at elevated carbon dioxide concentration ([CO2]); however, the molecular drivers for this increase are unknown. We investigated the molecular basis for changes in leaf development at elevated [CO2] using soybeans (Glycine max) grown under fully open air conditions at the Soybean Free Air CO2 Enrichment (SoyFACE) facility. The transcriptome responses of rapidly growing and fully expanded leaves to elevated [CO2] were investigated using cDNA microarrays. We identified 1,146 transcripts that showed a significant change in expression in growing versus fully expanded leaves. Transcripts for ribosomal proteins, cell cycle, and cell wall loosening, necessary for cytoplasmic growth and cell proliferation, were highly expressed in growing leaves. We further identified 139 transcripts with a significant [CO2] by development interaction. Clustering of these transcripts showed that transcripts involved in cell growth and cell proliferation were more highly expressed in growing leaves that developed at elevated [CO2] compared to growing leaves that developed at ambient [CO2]. The 327 [CO2]-responsive genes largely suggest that elevated [CO2] stimulates the respiratory breakdown of carbohydrates, which provides increased energy and biochemical precursors for leaf expansion and growth at elevated [CO2]. While increased photosynthesis and carbohydrate production at elevated [CO2] are well documented, this research demonstrates that at the transcript and metabolite level, respiratory breakdown of starch is also increased at elevated [CO2].

[1]  G. Churchill,et al.  Statistical design and the analysis of gene expression microarray data. , 2007, Genetical research.

[2]  L. Vodkin,et al.  Extraction of RNA from tissues containing high levels of procyanidins that bind RNA , 1994, Plant Molecular Biology Reporter.

[3]  F. Miglietta,et al.  Spatial and Temporal Effects of Free-Air CO2Enrichment (POPFACE) on Leaf Growth, Cell Expansion, and Cell Production in a Closed Canopy of Poplar1 , 2003, Plant Physiology.

[4]  S. Thitamadee,et al.  Microtubule defects and cell morphogenesis in the lefty1lefty2 tubulin mutant of Arabidopsis thaliana. , 2004, Plant & cell physiology.

[5]  O. H. Lowry,et al.  Enzymic Assay of 10−7 to 10−14 Moles of Sucrose in Plant Tissues , 1977 .

[6]  M. M. Christ,et al.  The effect of elevated CO2 on diel leaf growth cycle, leaf carbohydrate content and canopy growth performance of Populus deltoides , 2005 .

[7]  P. Curtis,et al.  A meta‐analysis of elevated [CO2] effects on soybean (Glycine max) physiology, growth and yield , 2002 .

[8]  U. Rascher,et al.  Functional dynamics of plant growth and photosynthesis--from steady-state to dynamics--from homogeneity to heterogeneity. , 2006, Plant, cell & environment.

[9]  Wilhelm Gruissem,et al.  Biochemistry & Molecular Biology of Plants , 2002 .

[10]  H. Heldt,et al.  Plant biochemistry and molecular biology , 1997 .

[11]  S. Long,et al.  Food for Thought: Lower-Than-Expected Crop Yield Stimulation with Rising CO2 Concentrations , 2006, Science.

[12]  S. Long,et al.  Respiratory Oxygen Uptake Is Not Decreased by an Instantaneous Elevation of [CO2], But Is Increased with Long-Term Growth in the Field at Elevated [CO2]1 , 2004, Plant Physiology.

[13]  F. Miglietta,et al.  Free‐air CO2 enrichment (FACE) of a poplar plantation: the POPFACE fumigation system , 2001 .

[14]  A. Rogers,et al.  Rising atmospheric carbon dioxide: plants FACE the future. , 2004, Annual review of plant biology.

[15]  F. Thibaud-Nissen,et al.  Microarrays for global expression constructed with a low redundancy set of 27,500 sequenced cDNAs representing an array of developmental stages and physiological conditions of the soybean plant , 2004, BMC Genomics.

[16]  Rishikesh Bhalerao,et al.  Molecular targets of elevated [CO2] in leaves and stems of Populus deltoides: implications for future tree growth and carbon sequestration. , 2006, Functional plant biology : FPB.

[17]  Ulrich Schurr,et al.  Nocturnal changes in leaf growth of Populus deltoides are controlled by cytoplasmic growth , 2006, Planta.

[18]  W. Liang,et al.  9) TM4 Microarray Software Suite , 2006 .

[19]  M. Paul,et al.  Products of leaf primary carbon metabolism modulate the developmental programme determining plant morphology. , 2006, Journal of experimental botany.

[20]  F. Miglietta,et al.  Leaf area is stimulated in Populus by free air CO2 enrichment (POPFACE), through increased cell expansion and production , 2001 .

[21]  S. Duplessis,et al.  Gene expression patterns of trembling aspen trees following long-term exposure to interacting elevated CO2 and tropospheric O3. , 2005, The New phytologist.

[22]  P. Garosi,et al.  DAG, a gene required for chloroplast differentiation and palisade development in Antirrhinum majus. , 1996, The EMBO journal.

[23]  Glycine max leaflets lack a base-tip gradient in growth rate , 2005, Journal of Plant Research.

[24]  Robert Turgeon,et al.  The Sink-Source Transition in Leaves , 1989 .

[25]  G. Barcaccia,et al.  Alfalfa Mob1-like proteins are involved in cell proliferation and are localized in the cell division plane during cytokinesis. , 2006, Experimental cell research.

[26]  W. Gregory.  Smaller than predicted increase in aboveground net primary production and yield of field-grown soybean under fully open-air (CO 2 ) elevation , 2005 .

[27]  G. Taylor,et al.  Elevated CO2 and plant growth: cellular mechanisms and responses of whole plants , 1994 .

[28]  A I Saeed,et al.  TM4: a free, open-source system for microarray data management and analysis. , 2003, BioTechniques.

[29]  M. Berenbaum,et al.  SoyFACE: the Effects and Interactions of Elevated [CO2] and [O3] on Soybean , 2006 .

[30]  R. Nelson,et al.  Smaller than predicted increase in aboveground net primary production and yield of field‐grown soybean under fully open‐air [CO2] elevation , 2005 .

[31]  J. Bunce.  Leaf Elongation in Relation to Leaf Water Potential in Soybean , 1977 .

[32]  G. Casadoro,et al.  Differential expression of genes in apical and basal tissues of expanding tobacco leaves , 2004 .

[33]  E. Herman,et al.  Binding-protein expression is subject to temporal, developmental and stress-induced regulation in terminally differentiated soybean organs , 1995, Planta.

[34]  S. Long,et al.  How does elevated CO2 or ozone affect the leaf-area index of soybean when applied independently? , 2006, The New phytologist.

[35]  Keith Roberts,et al.  "Big it up": endoreduplication and cell-size control in plants. , 2003, Current opinion in plant biology.

[36]  E. Neufeld,et al.  CARBOHYDRATE METABOLISM. , 1965, Annual review of biochemistry.

[37]  Alison M. Smith,et al.  Starch degradation. , 2005, Annual Review of Plant Biology.

[38]  S. Duplessis,et al.  Gene expression patterns of trembling aspen trees following long-term exposure to interacting elevated CO2 and tropospheric O3. , 2005, The New phytologist.

[39]  Hong Li,et al.  Differential Gene Expression in Response to Hydrogen Peroxide and the Putative PerR Regulon of Synechocystis sp. Strain PCC 6803 , 2004, Journal of bacteriology.

[40]  M. Stitt,et al.  ADP-Glucose Pyrophosphorylase Is Activated by Posttranslational Redox-Modification in Response to Light and to Sugars in Leaves of Arabidopsis and Other Plant Species1[w] , 2003, Plant Physiology.

[41]  G. Taylor,et al.  Long‐term acclimation of leaf production, development, longevity and quality following 3 yr exposure to free‐air CO2 enrichment during canopy closure in Populus , 2004 .

[42]  D. Nevins,et al.  New perspectives on the endo-beta-glucanases of glycosyl hydrolase Family 17. , 2000, International journal of biological macromolecules.

[43]  J. McGrath,et al.  Hourly and seasonal variation in photosynthesis and stomatal conductance of soybean grown at future CO(2) and ozone concentrations for 3 years under fully open-air field conditions. , 2006, Plant, cell & environment.

[44]  L. McIntyre,et al.  Combining mapping and arraying: An approach to candidate gene identification , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[45]  G. S. Avery,.  STRUCTURE AND DEVELOPMENT OF THE TOBACCO LEAF , 1933 .

[46]  Gail Taylor,et al.  The transcriptome of Populus in elevated CO2. , 2005, The New phytologist.

[47]  A. Rogers,et al.  Leaf photosynthesis and carbohydrate dynamics of soybeans grown throughout their life‐cycle under Free‐Air Carbon dioxide Enrichment , 2004 .

[48]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[49]  M. Stitt,et al.  Increased C availability at elevated carbon dioxide concentration improves N assimilation in a legume. , 2006, Plant, cell & environment.