Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

The effects of resource availability and environmental conditions on genetic rankings for carbon isotope discrimination during growth in tomato and rice

Jonathan P. Comstock A F , Susan R. McCouch A , Bjorn C. Martin B , Charles G. Tauer C , Todd J. Vision D , Yunbi Xu A and Roman C. Pausch E
+ Author Affiliations
- Author Affiliations

A Department of Plant Breeding, Cornell University, Ithaca, NY 14853, USA.

B Department of Plant and Soil Sciences, Oklahoma State University, Stillwater, OK 74078, USA.

C Department of Forestry, Oklahoma State University, Stillwater, OK 74078, USA.

D Department of Biology, University of North Carolina, Campus Box 3280 Chapel Hill, NC 27599, USA.

E Boyce Thompson Institute for Plant Research at Cornell University, Ithaca, NY 14853, USA.

F Corresponding author. Email: JPC8@cornell.edu

Functional Plant Biology 32(12) 1089-1105 https://doi.org/10.1071/FP05117
Submitted: 17 May 2005  Accepted: 29 July 2005   Published: 1 December 2005

Abstract

Carbon isotope discrimination (Δ) is frequently used as an index of leaf intercellular CO2 concentration (ci) and variation in photosynthetic water use efficiency. In this study, the stability of Δ was evaluated in greenhouse-grown tomato and rice with respect to variable growth conditions including temperature, nutrient availability, soil flooding (in rice), irradiance, and root constriction in small soil volumes. Δ exhibited several characteristics indicative of contrasting set-point behaviour among genotypes of both crops. These included generally small main environmental effects and lower observed levels of genotype-by-environment interaction across the diverse treatments than observed in associated measures of relative growth rate, photosynthetic rate, biomass allocation pattern, or specific leaf area. Growth irradiance stood out among environmental parameters tested as having consistently large main affects on Δ for all genotypes screened in both crops. We suggest that this may be related to contrasting mechanisms of stomatal aperture modulation associated with the different environmental variables. For temperature and nutrient availability, feedback processes directly linked to ci and / or metabolite pools associated with ci may have played the primary role in coordinating stomatal conductance and photosynthetic capacity. In contrast, light has a direct effect on stomatal aperture in addition to feedback mediated through ci.


Acknowledgments

We wish to thank Christine Fleet and Wendy Vonhof for major contributions in data collection and analysis, Brian Gollands for figure preparation, and Paul King for coordination and mentoring of high school and undergraduate interns. In particular, Rebecca Rudicell collected data for the Keeling plots relating δ13C of greenhouse air to atmospheric [CO2]; Shaan Ghandi and Leonora Ballantyne did repeated size measures for growth analysis and Anna Nowogrodski and Laura Vineyard assisted with gas-exchange measurements. This work was supported by the National Science Foundation (Plant Genome Research Project Grant DBI-0110069, Genomic Analysis of Plant Water Use Efficiency.


References


Ares A, Fownes JH, Sun W (2000) Genetic differentiation of intrinsic water-use efficiency in the Hawaiian native Acacia koa. International Journal of Plant Sciences 161( ), 909–915.
CrossRef |

Assmann SM, Palade GE (1993) Signal transduction in guard cells. Annual Review of Cell Biology 9( ), 345–375.
CrossRef | PubMed |

Bacon, MA (2004). Biological Science Series. ‘Water use efficiency in plant biology.’ (Blackwell Publishing Ltd: Carlton)

Ball JT, Woodrow IE, Berry JA (1987) A model predicting stomatal conductance and its contribution to the control of photosynthesis under different environmental conditions. Progress in Photosynthetic Research 4( ), 221–228.

Barbour MM, Farquhar GD (2000) Relative humidity- and ABA-induced variation in carbon and oxygen isotope ratios of cotton leaves. Plant, Cell & Environment 23( ), 473–485.
CrossRef |

Brownlee C (2001) The long and the short of stomatal density signals. Trends in Plant Science 6( ), 441–442.
CrossRef | PubMed |

Brück H, Jureit C, Hermann M, Schulz A, Sattelmacher B (2001) Effects of water and nitrogen supply on water use efficiency and carbon isotope discrimination in edible canna (Canna edulis Ker-Gawler). Plant Biology 3( ), 326–334.
CrossRef |

Brugnoli, E ,  and  Farquhar, GD (1999). Photosynthetic fractionation of carbon isotopes. In ‘Photosynthesis: physiology and metabolism’. pp. 399–434. (Kluwer Academic Publishers: Boston)

Budiman MA, Mao L, Wood TC, Wing RA (2000) A deep-coverage tomato BAC library and prospects toward development of an STC framework for genome sequencing. Genome Research 10( ), 129–136.
PubMed |


Cabuslay GS, Ito O, Alejar AA (2002) Physiological evaluation of responses of rice (Oryza sativa L.) to water deficit. Plant Science 163( ), 815–827.
CrossRef |

Carelli MLC, Fahl JI, Trivelin PCO, Queiroz Voltan RB (1999) Carbon isotope discrimination and gas exchange in Coffea species grown under different irradiance regimes. Revista Brasileira de Fisiologia Vegetal 11( ), 63–68.

Comstock JP (2002) Hydraulic and chemical signalling in the control of stomatal conductance and transpiration. Journal of Experimental Botany 53( ), 195–200.
CrossRef | PubMed |

Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2002) Improving intrinsic water-use efficiency and crop yield. Crop Science 42( ), 122–131.
PubMed |


Craufurd PQ, Wheeler TR, Ellis RH, Summerfield RJ, Williams JH (1999) Effect of temperature and water deficit on water-use efficiency, carbon isotope discrimination, and specific leaf area in peanut. Crop Science 39( ), 136–142.

Cregg BM, Olivas Garcia JM, Hennessey TC (2000) Provenance variation in carbon isotope discrimination of mature ponderosa pine trees at two locations in the Great Plains. Canadian Journal of Forest Research 30( ), 428–439.
CrossRef |

DaMatta FM, Loos RA, Silva EA, Loureiro ME, Ducatti C (2002) Effects of soil water deficit and nitrogen nutrition on water relations and photosynthesis of pot-grown Coffea canephora Pierre. Trees 16( ), 555–558.
CrossRef |

DesRochers A, van den Driessche R, Thomas BR (2003) Nitrogen fertilization of trembling aspen seedlings grown on soils of different pH. Canadian Journal of Forest Research 33( ), 552–560.
CrossRef |

Dietrich P, Sanders D, Hedrich R (2001) The role of ion channels in light-dependent stomatal opening. Journal of Experimental Botany 52( ), 1959–1967.
CrossRef | PubMed |

Dingkuhn M, Cruz RT, O’Toole JC, Turner NC, Doerffling K (1991a) Responses of seven diverse rice cultivars to water deficits III. Accumulation of abscisic acid and proline in relation to leaf water-potential and osmotic adjustment. Field Crops Research 27( ), 103–118.
CrossRef |

Dingkuhn M, Farquhar GD, De Datta SK, O’Toole JC (1991b) Discrimination of carbon-13 among upland rices having different water use efficiencies. Australian Journal of Agricultural Research 42( ), 1123–1132.
CrossRef |

Ehleringer JR, Field CB, Lin ZF, Kuo CY (1986) Leaf carbon isotope and mineral composition in subtropical plants along an irradiance cline. Oecologia 70( ), 520–526.
CrossRef |

Ehleringer JR, White JW, Johnson DA, Brick M (1990) Carbon isotope discrimination photosynthetic gas exchange and transpiration efficiency in beans and range grasses. Acta Oecologica 11( ), 611–625.

Eshed Y, Zamir D (1994) A genomic library of Lycopersicon pennellii in L. esculentum: a tool for fine mapping of genes. Euphytica 79( ), 175–179.
CrossRef |

Evans JR, von Caemmerer S (1996) Carbon dioxide diffusion inside leaves. Plant Physiology 110( ), 339–346.
PubMed |


Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Australian Journal of Plant Physiology 11( ), 539–552.

Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40( ), 503–537.
CrossRef |

Franks PJ, Farquhar GD (1999) A relationship between humidity response, growth form and photosynthetic operating point in C3 plants. Plant, Cell & Environment 22( ), 1337–1349.
CrossRef |

Geber MA, Dawson TE (1997) Genetic variation in stomatal and biochemical limitations to photosynthesis in the annual plant, Polygonum arenastrum. Oecologia 109( ), 535–546.
CrossRef |

Ghashghaie J, Badeck FW, Lanigan G, Nogues S, Tcherkez G, Deleens E, Cornic G, Griffiths H (2003) Carbon isotope fractionation during dark respiration and photorespiration in C3 plants. Phytochemistry Reviews 2( ), 145–161.
CrossRef |

Goff SA, Ricke D, Lan T-H, Presting G, Wang R , et al. (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296( ), 92–100.
CrossRef | PubMed |

Guo S, Brück H, Sattelmacher B (2002) Effects of supplied nitrogen form on growth and water uptake of French bean (Phaseolus vulgaris L.) plants: nitrogen form and water uptake. Plant and Soil 239( ), 267–275.
CrossRef |

Hall AE, Thiaw S, Krieg DR (1994) Consistency of genotypic ranking for carbon isotope discrimination by cowpea grown in tropical and subtropical zones. Field Crops Research 36( ), 125–131.
CrossRef |

Hamerlynck EP, Huxman TE, McAuliffe JR, Smith SD (2004) Carbon isotope discrimination and foliar nutrient status of Larrea tridentata (creosote bush) in contrasting Mojave Desert soils. Oecologia 138( ), 210–215.
CrossRef | PubMed |

Hanba YT, Mori S, Lei TT, Koike T, Wada E (1997) Variations in leaf delta-13C along a vertical profile of irradiance in a temperate Japanese forest. Oecologia 110( ), 253–261.
CrossRef |

Huang N, Parco A, Mew T, Magpantay G, McCouch S, Guiderdoni E, Xu J, Subudhi P, Angeles ER, Khush GS (1997) RFLP mapping of isozymes, RAPD and QTLs for grain shape, brown planthopper resistance in a doubled haploid rice population. Molecular Breeding 3( ), 105–113.
CrossRef |

Hubick KT, Shorter R, Farquhar GD (1988) Heritability and genotype × environment interactions of carbon isotope discrimination and transpiration efficiency in peanut Arachis hypogaea L. Australian Journal of Plant Physiology 15( ), 799–814.

Huxman TE, Monson RK (2003) Stomatal responses of C3, C3–C4 and C4 Flaveria species to light and intercellular CO2 concentration: implications for the evolution of stomatal behaviour. Plant, Cell & Environment 26( ), 313–322.
CrossRef |

Ishimaru K, Yano M, Aoki N, Ono K, Hirose T, Lin SY, Monna L, Sasaki T, Ohsugi R (2001) Toward the mapping of physiological and agronomic characters on a rice function map: QTL analysis and comparison between QTLs and expressed sequence tags. Theoretical and Applied Genetics 102( ), 793–800.
CrossRef |

Keeling CD (1958) The concentration and isotopic abundances of atmospheric carbon dioxide in rural areas. Geochimica et Cosmochimica Acta 13( ), 322–334.
CrossRef |

Korner C, Scheel JA, Bauer H (1979) Maximum leaf diffusive conductance in vascular plants. Photosynthetica 13( ), 45–82.

Larcher, W (1995). ‘Physiological plant ecology.’ (Springer-Verlag: Berlin)

Le Roux D, Stock WD, Bond WJ, Maphanga D (1996) Dry mass allocation, water use efficiency and delta-13C in clones of Eucalyptus grandis, E. grandis × camaldulensis and E. grandis × nitens grown under two irrigation regimes. Tree Physiology 16( ), 497–502.
PubMed |


Lin S, Sasaki T, Yano M (1998) Mapping quantitative trait loci controlling seed dormancy and heading date in rice, Oryza sativa L., using backcross inbred lines. Theoretical and Applied Genetics 96( ), 997–1003.
CrossRef |

Livingston NJ, Guy RD, Sun ZJ, Ethier GJ (1999) The effects of nitrogen stress on the stable carbon isotope composition, productivity and water use efficiency of white pine (Picea glauca (Moench) Voss) seedlings. Plant, Cell & Environment 22( ), 281–289.
CrossRef |

Madhavan S, Treichel I, O’Leary MH (1991) Effects of relative humidity on carbon isotope fractionation in plants. Botanica Acta 104( ), 292–294.

Martin B, Nienhuis J, King G, Schaefer A (1989) Restriction fragment length polymorphisms associated with water use efficiency in tomato. Science 243( ), 1725–1728.

Martin B, Tauer CG, Lin RK (1999) Carbon isotope discrimination as a tool to improve water-use efficiency in tomato. Crop Science 39( ), 1775–1783.

Matzner S, Comstock J (2001) The temperature dependence of shoot hydraulic resistance: Implications for stomatal behaviour and hydraulic limitation. Plant, Cell & Environment 24( ), 1299–1307.
CrossRef |

McKay JK, Richards JH, Mitchell Olds T (2003) Genetics of drought adaptation in Arabidopsis thaliana: I. Pleiotropy contributes to genetic correlations among ecological traits. Molecular Ecology 12( ), 1137–1151.
CrossRef | PubMed |

Merah O, Monneveux P, Nachit M, Deleens E (1999) The carbon isotope composition, an integrative criterion of stomatal functioning: application to durum wheat improvement under Mediterranean conditions. Cahiers Agricultures 8( ), 37–47.

Monforte AJ, Tanksley SD (2000) Development of a set of near isogenic and backcross recombinant inbred lines containing most of the Lycopersicon habrochaites genome in a L. esculentum genetic background: a tool for gene mapping and gene discovery. Genome 43( ), 803–813.
CrossRef | PubMed |

Morecroft MD, Woodward FI (1996) Experiments on the causes of altitudinal differences in the leaf nutrient contents, size and delta-13C of Alchemilla alpina. New Phytologist 134( ), 471–479.

Mott KA (1988) Do stomata respond to CO2 concentrations other than intercellular. Plant Physiology 86( ), 200–203.

Mott KA (1990) Sensing of atmospheric CO2 by plants. Plant, Cell & Environment 13( ), 731–737.

Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. Journal of Experimental Botany 52( ), 1383–1400.
CrossRef | PubMed |

Pennington RE, Tischler CR, Johnson HB, Polley HW (1999) Genetic variation for carbon isotope composition in honey mesquite (Prosopis glandulosa). Tree Physiology 19( ), 583–589.
PubMed |


Ponton S, Dupouey JL, Breda N, Dreyer E (2002) Comparison of water-use efficiency of seedlings from two sympatric oak species: genotype × environment interactions. Tree Physiology 22( ), 413–422.
PubMed |


Prasolova NV, Xu ZH, Lundkvist K, Farquhar GD, Dieters MJ, Walker S, Saffigna PG (2003) Genetic variation in foliar carbon isotope composition in relation to tree growth and foliar nitrogen concentration in clones of the F1 hybrid between slash pine and Caribbean pine. Forest Ecology and Management 172( ), 145–160.
CrossRef |

Rao RCN, Udaykumar M, Farquhar GD, Talwar HS, Prasad TG (1995) Variation in carbon isotope discrimination and its relationship to specific leaf area and ribulose-1,5-bisphosphate carboxylase content in groundnut genotypes. Australian Journal of Plant Physiology 22( ), 545–551.

Raven JA, Farquhar GD (1990) The influence of N metabolism and organic acid synthesis on the natural abundance of isotopes of carbon in plants. New Phytologist 116( ), 505–529.

Rebetzke GJ, Condon AG, Richards RA, Farquhar GD (2002) Selection for reduced stable carbon isotope discrimination increases aerial biomass and grain yield of rainfed bread wheat. Crop Science 42( ), 739–745.

Reich PB, Ellsworth DS, Walters MB (1998) Leaf structure (specific leaf area) modulates photosynthesis–nitrogen relations: evidence from within and across species and functional groups. Functional Ecology 12( ), 948–958.
CrossRef |

Reich PB, Ellsworth DS, Walters MB, Vose JM, Gresham C, Volin JC, Bowman WD (1999) Generality of leaf trait relationships: a test across six biomes. Ecology 80( ), 1955–1969.

Richards RA, Rebetzke GJ, Condon AG, van Herwaarden AF (2002) Breeding opportunities for increasing the efficiency of water use and crop yield in temperate cereals. Crop Science 42( ), 111–121.
PubMed |


Sage RF (2000) How plants sense, signal, and respond to carbon dioxide. American Zoologist 40( ), 1194–1195.

Sanchez Diaz M, Garcia JL, Antolin MC, Araus JL (2002) Effects of soil drought and atmospheric humidity on yield, gas exchange, and stable carbon isotope composition of barley. Photosynthetica 40( ), 415–421.
CrossRef |

Sperry JS, Hacke UG, Oren R, Comstock JP (2002) Water deficits and hydraulic limits to leaf water supply. Plant, Cell & Environment 25( ), 251–263.
CrossRef | PubMed |

Stiller V, Lafitte HR, Sperry JS (2003) Hydraulic properties of rice and the response of gas exchange to water stress. Plant Physiology 132( ), 1698–1706.
CrossRef | PubMed |

Teulat B, Merah O, Sirault X, Borries C, Waugh R, This D (2002) QTLs for grain carbon isotope discrimination in field-grown barley. Theoretical and Applied Genetics 106( ), 118–126.
PubMed |


Turner, NC (1993). Water use efficiency of crop plants: potential for improvement. In ‘International crop science, I’. pp. 75–82. (Crop Science Society of America Inc.: Madison)

Udayakumar M, Sheshshayee MS, Nataraj KN, Madhava HB, Devendra R, Hussain ISA, Prasad TG (1998) Why has breeding for water use efficiency not been successful? An analysis and alternate approach to exploit this trait for crop improvement. Current Science (Bangalore) 74( ), 994–1000.

Van der Hoeven R, Ronning C, Giovannoni J, Martin G, Tanksley SD (2002) Deductions about the number, organization and evolution of genes in the tomato genome based on analysis of a large EST collection and selective genomic sequencing. The Plant Cell 14( ), 1441–1456.
CrossRef | PubMed |

Virgona JM, Farquhar GD (1996) Genotypic variation in relative growth rate and carbon isotope discrimination in sunflower is related to photosynthetic capacity. Australian Journal of Plant Physiology 23( ), 227–236.

White JW, Castillo JA, Ehleringer JR, Garcia CJA, Singh SP (1994) Relations of carbon isotope discrimination and other physiological traits to yield in common bean (Phaseolus vulgaris) under rainfed conditions. Journal of Agricultural Science 122( ), 275–284.

Wong SC, Cowan IR, Farquhar GD (1979) Stomatal conductance correlates with photosynthetic capacity. Nature 282( ), 424–426.
CrossRef |

Zacharisen MH, Brick MA, Fisher AG, Ogg JB, Ehleringer JR (1999) Relationships between productivity and carbon isotope discrimination among dry bean lines and F2 progeny. Euphytica 105( ), 239–250.
CrossRef |








Rent Article (via Deepdyve) Export Citation Cited By (15)