Abstract
Growth chambers allow measurement of phenotypic differences among genotypes under controlled environment conditions. However, unintended variation in growth chamber air CO2 concentration ([CO2]) may affect the expression of diverse phenotypic traits, and genotypes may differ in their response to variation in [CO2]. We monitored [CO2] and quantified phenotypic responses of 22 Brassica rapa genotypes in growth chambers with either standard or enhanced venting. [CO2] in chambers with standard venting dropped to 280 μmol mol−1 during the period of maximum canopy development, ~80 μmol mol−1 lower than in chambers with enhanced venting. The stable carbon isotope ratio of CO2 in chamber air (δ13Cair) was negatively correlated with [CO2], suggesting that photosynthesis caused observed [CO2] decreases. Significant genotype × chamber-venting interactions were detected for 12 of 20 traits, likely due to differences in the extent to which [CO2] changed in relation to genotypes’ phenology or differential sensitivity of genotypes to low [CO2]. One trait, 13C discrimination (δ13C), was particularly influenced by unaccounted-for fluctuations in δ13Cair and [CO2]. Observed responses to [CO2] suggest that genetic variance components estimated in poorly vented growth chambers may be influenced by the expression of genes involved in CO2 stress responses; genotypic values estimated in these chambers may likewise be misleading such that some mapped quantitative trait loci may regulate responses to CO2 stress rather than a response to the environmental factor of interest. These results underscore the importance of monitoring, and where possible, controlling [CO2].
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References
Andaya VC, Mackill DJ (2003a) Mapping of QTLs associated with cold tolerance during the vegetative stage in rice. J Exp Bot 54:2579–2585
Andaya VC, Mackill DJ (2003b) QTLs conferring cold tolerance at the booting stage of rice using recombinant inbred lines from a japonica × indica cross. Theor Appl Genet 106:1084–1090
Bernier PY, Stewart JD, Hogan GD (1994) Quantifying the uncontrolled CO2 dynamics of growth chambers. J Exp Bot 45:1143–1146
Berry SC, Varney GT, Flanagan LB (1997) Leaf delta C13 in Pinus resinosa trees and understory plants: variation associated with light and CO2 gradients. Oecologia 109:499–506
Bloom AJ, Smart DR, Nguyen DT, Searles PS (2002) Nitrogen assimilation and growth of wheat under elevated carbon dioxide. Proc Natl Acad Sci USA 99:1730–1735
Broadmeadow MSJ, Griffiths H, Maxwell C, Borland AM (1992) The carbon isotope ratio of plant organic material reflects temporal and spatial variations in CO2 within tropical forest formations in Trinidad. Oecologia 89:435–441
Brouillette LC, Rosenthal DM, Rieseberg LH, Lexer C, Malmberg RL, Donovan LA (2007) Genetic architecture of leaf ecophysiological traits in Helianthus. J Hered 98:142–146
Comstock JP, McCouch SR, Martin BC, Tauer CG, Vision TJ, Xu YB, Pausch RC (2005) The effects of resource availability and environmental conditions on genetic rankings for carbon isotope discrimination during growth in tomato and rice. Funct Plant Biol 32:1089–1105
Corbesier L, Coupland G (2005) Photoperiodic flowering of Arabidopsis: integrating genetic and physiological approaches to characterization of the floral stimulus. Plant Cell Environ 28:54–66
Dechaine JM, Johnston JA, Brock MT, Weinig C (2007) Constraints on the evolution of adaptive plasticity: costs of plasticity to density are expressed in segregating progenies. New Phytol 176:874–882
Degenkolbe T, Do PT, Zuther E, Repsilber D, Walther D, Hincha DK, Kohl KI (2009) Expression profiling of rice cultivars differing in their tolerance to long-term drought stress. Plant Mol Biol 69:133–153
Dippery JK, Tissue DT, Thomas RB, Strain BR (1995) Effects of low and elevated CO2 on C3 and C4 annuals. I. Growth and biomass allocation. Oecologia 101:13–20
Ehleringer JR (1993) Carbon isotope variation in Encelia farinosa: implications for growth, competition, and drought survival. Oecologia 95:340–346
Etheridge DM, Steele LP, Langenfelds RL, Francey RJ, Barnola J-M, Morgan VI (1996) Natural and anthropogenic changes in atmospheric CO2 over the last 1000 years from air in Antarctic ice and firn. J Geophys Res 101:4115–4128
Farquhar GD, Lloyd J (1993) Carbon and oxygen isotope effects in the exchange of carbon dioxide between terrestrial plants and the atmosphere. In: Hall AE, Farquhar GD (eds) Stable isotopes in plant carbon–water relations. Academic Press, San Diego, pp 47–70
Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345
Farquhar GD, Caemmerer SV, Berry JA (1980) A biochemical-model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90
Farquhar GD, Oleary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the inter-cellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9:121–137
Farquhar GD, Hubick KT, Condon AG, Richards RA (1988) Carbon isotope fractionation and plant water-use efficiency. In: Rundel PW, Ehleringer JR, Nogy KA (eds) Stable isotopes in ecological research. Springer, New York, pp 21–40
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537
Funatsuki H, Matsuba S, Kawaguchi K, Murakami T, Sato Y (2004) Methods for evaluation of soybean chilling tolerance at the reproductive stage under artificial climatic conditions. Plant Breed 123:558–563
Hall NM, Griffiths H, Corlett JA, Jones HG, Lynn J, King GJ (2005) Relationships between water-use traits and photosynthesis in Brassica oleracea resolved by quantitative genetic analysis. Plant Breed 124:557–564
Hausmann NJ, Juenger TE, Sen S, Stowe KA, Dawson TE, Simms EL (2005) Quantitative trait loci affecting δC13 and response to differential water availability in Arabidopsis thaliana. Evol Int J Org Evol 59:81–96
Ismail AM, Hall AE (1993) Carbon isotope discrimination and gas exchange of Cowpea accessions and hybrids. Crop Sci 33:788–793
Jiao SX, Emmanuel H, Guikema JA (2004) High light stress inducing photoinhibition and protein degradation of photosystem I in Brassica rapa. Plant Sci 167:733–741
Juenger TE, McKay JK, Hausmann N, Keurentjes JJB, Sen S, Stowe KA, Dawson TE, Simms EL, Richards JH (2005) Identification and characterization of QTL underlying whole-plant physiology in Arabidopsis thaliana: δC13, stomatal conductance and transpiration efficiency. Plant Cell Environ 28:697–708
Lacey EP (1996) Parental effects in Plantago lanceolata L. 1. A growth chamber experiment to examine pre- and postzygotic temperature effects. Evol Int J Org Evol 50:865–878
Long SP, Bernacchi CJ (2003) Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. J Exp Bot 54:2393–2401
Lou QJ, Chen L, Sun ZX, Xing YZ, Li J, Xu XY, Mei HW, Luo LJ (2007) A major QTL associated with cold tolerance at seedling stage in rice (Oryza sativa L.). Euphytica 158:87–94
Masle J, Gilmore SR, Farquhar GD (2005) The ERECTA gene regulates plant transpiration efficiency in Arabidopsis. Nature 436:866–870
McKay JK, Richards JH, Nemali KS, Sen S, Mitchell-Olds T, Boles S, Stahl EA, Wayne T, Juenger TE (2008) Genetics of drought adaptation in Arabidopsis thaliana. II. QTL analysis of a new mapping population, Kas-1 × Tsu-1. Evol Int J Org Evol 62:3014–3026
Medlyn BE, Dreyer E, Ellsworth D, Forstreuter M, Harley PC, Kirschbaum MUF, Le Roux X, Montpied P, Strassemeyer J, Walcroft A et al (2002) Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data. Plant Cell Environ 25:1167–1179
Neftel A, Oeschger H, Schwander J, Stauffer B, Zumbrunn R (1982) Ice core sample measurements give atmospheric CO2 content during the past 40,000 year. Nature 295:220–223
Oleary MH (1988) Carbon isotopes in photosynthesis. Bioscience 38:328–336
Onouchi H, Coupland G (1998) The regulation of flowering time of Arabidopsis in response to daylength. J Plant Res 111:271–275
Panek JA, Waring RH (1995) Carbon-isotope variation in Douglas-fir foliage: improving the delta C13-climate relationship. Tree Physiol 15:657–663
Patterson DT, Hite JL (1975) A CO2 monitoring and control system for plant growth chambers. Ohio J Sci 75:190–193
Peet MM, Krizek DT (1997) Carbon dioxide. In: Langhans RW, Tibbitts TW (eds) Plant growth chamber handbook. North Central Regional Research Committee Publication Number 340, Ames, IA, pp 65–79
Polley HW, Johnson HB, Marino BD, Mayeux HS (1993) Increase in C3 plant water-use efficiency and biomass over glacial to present CO2 concentrations. Nature 361:61–64
Potvin C, Lechowicz MJ, Bell G, Schoen D (1990) Spatial, temporal, and species-specific patterns of heterogeneity in growth chamber experiments. Can J Bot 68:499–504
Prakash S, Hinata K (1980) Taxonomy, cytogenetics and origin of crop Brassicas, a review. Opera Bot 55:1–57
Rasband WS (1997–2007) ImageJ. National Institutes of Health, Bethesda, MD
Rytter RM (2005) Water use efficiency, carbon isotope discrimination and biomass production of two sugar beet varieties under well-watered and dry conditions. J Agron Crop Sci 191:426–438
Sage RF (1995) Was low atmospheric CO2 during the Pleistocene a limiting factor for the origin of agriculture? Global Change Biol 1:93–106
Sage RF, Coleman JR (2001) Effects of low atmospheric CO2 on plants: more than a thing of the past. Trends Plant Sci 6:18–24
Sato T, Ueda T, Fukuta Y, Kumagai T, Yano M (2003) Mapping of quantitative trait loci associated with ultraviolet-B resistance in rice (Oryza sativa L.). Theor Appl Genet 107:1003–1008
Schauer AJ, Lai C-T, Bowling DR, Ehleringer JR (2003) An automated sampler for collection of atmospheric trace gas samples for stable isotope analyses. Agric For Meteorol 118:113–124
Seibt U, Rajabi A, Griffiths H, Berry J (2008) Carbon isotopes and water use efficiency: sense and sensitivity. Oecologia 155:441–454
Sharkey TD (1988) Estimating the rate of photorespiration in leaves. Physiol Plant 73:147–152
Sternberg LDL, Mulkey SS, Wright SJ (1989) Ecological interpretation of leaf carbon isotope ratios-influence of respired carbon dioxide. Ecology 70:1317–1324
Takai T, Fukuta Y, Sugimoto A, Shiraiwa T, Horie T (2006) Mapping of QTLs controlling carbon isotope discrimination in the photosynthetic system using recombinant inbred lines derived from a cross between two different rice (Oryza sativa L.) cultivars. Plant Product Sci 9:271–280
Tasma IM, Lorenzen LL, Green DE, Shoemaker RC (2001) Mapping genetic loci for flowering time, maturity, and photoperiod insensitivity in soybean. Mol Breed 8:25–35
Thumma BR, Naidu BP, Chandra A, Cameron DF, Bahnisch LM, Liu CJ (2001) Identification of causal relationships among traits related to drought resistance in Stylosanthes scabra using QTL analysis. J Exp Bot 52:203–214
Tibbitts TW, Krizek DT (1978) Carbon dioxide. In: Langhans R (ed) Growth chamber manual: environment control for plants. Cornell University Press, Ithaca, NY
Tissue DT, Griffin KL, Thomas RB, Strain BR (1995) Effects of low and elevated CO2 on C3 and C4 annuals. II. Photosynthesis and leaf biochemistry. Oecologia 101:21–28
Ward JK, Strain BR (1997) Effects of low and elevated CO2 partial pressure on growth and reproduction of Arabidopsis thaliana from different elevations. Plant Cell Environ 20:254–260
Welcker C, Boussuge B, Bencivenni C, Ribaut JM, Tardieu F (2007) Are source and sink strengths genetically linked in maize plants subjected to water deficit? A QTL study of the responses of leaf growth and of Anthesis-Silking Interval to water deficit. J Exp Bot 58:339–349
Wheeler RM (1992) Gas-exchange measurements using a large, closed plant growth chamber. HortScience 27:777–780
Ziska LH (2003) Evaluation of the growth response of six invasive species to past, present and future atmospheric carbon dioxide. J Exp Bot 54:395–404
Acknowledgments
The authors thank Wei Sun, Amy Hemenway, and Kusum Naithani for assistance with data collection, and Marcus T. Brock for assistance with data analyses. This research was supported by NSF grant DBI 0605736.
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Communicated by D. Lightfoot.
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Edwards, C.E., Haselhorst, M.S.H., McKnite, A.M. et al. Genotypes of Brassica rapa respond differently to plant-induced variation in air CO2 concentration in growth chambers with standard and enhanced venting. Theor Appl Genet 119, 991–1004 (2009). https://doi.org/10.1007/s00122-009-1103-5
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DOI: https://doi.org/10.1007/s00122-009-1103-5