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

Genetic variation for leaf carbon isotope discrimination and its association with transpiration efficiency in canola (Brassica napus)

Shek M. Hossain A D , Josette Masle B , Andrew Easton C E , Malcolm N. Hunter A , Ian D. Godwin A , Graham D. Farquhar B and Christopher J. Lambrides https://orcid.org/0000-0002-5543-1065 A F
+ Author Affiliations
- Author Affiliations

A The University of Queensland, School of Agriculture and Food Sciences, Brisbane, Qld 4072, Australia.

B Plant Sciences, Research School of Biology, Australian National University, ACT 2601, Australia.

C Advanta Seeds Pty Ltd, 268 Anzac Avenue, Toowoomba, QLD 4350, Australia.

D Present address: CSIRO Agriculture and Food, Building 101, Clunies Ross Street, Black Mountain, ACT 2601, Australia.

E Present address: Natural Resource Management (NRM) North, PO Box 1224, Launceston, TAS 7250, Australia.

F Corresponding author. Email: chris.lambrides@uq.edu.au

Functional Plant Biology 47(4) 355-367 https://doi.org/10.1071/FP19256
Submitted: 30 August 2019  Accepted: 1 December 2019   Published: 5 March 2020

Abstract

Drought is a major constraint to canola production around the world. There is potential for improving crop performance in dry environments by selecting for transpiration efficiency (TE). In this work we investigated TE by studying its genetic association with carbon isotope discrimination (Δ) and other traits, e.g. specific leaf weight (SLW) and leaf chlorophyll content (SPAD). Among the 106 canola genotypes – including open-pollinated, hybrid, inbred types and cytoplasmic variants – tested in the field and glasshouse there was significant genotypic variation for TE, Δ, plant total dry weight, SLW and SPAD. Strong negative correlations were observed between TE and Δ (–0.52 to –0.76). Negative correlations between Δ and SLW or SPAD (–0.43 to –0.78) and smaller but significant positive correlations between TE and SLW or SPAD (0.23 to 0.30) suggested that photosynthetic capacity was, in part, underpinning the variation in TE. A cytoplasmic contribution to genetic variation in TE or Δ in canola was also observed with Triazine tolerant types having low TE and high Δ. This study showed that Δ has great potential for selecting canola germplasm with improved TE.

Additional keywords: C3 photosynthesis, drought tolerance.


References

Arntzen CJ, Pfister K, Steinback KE (1982) The mechanism of chloroplast triazine resistance: alterations in the site of herbicide action. In ‘Herbicide resistance in plants’. (Eds HM LeBaron, J Gressel) pp. 185–214. (John Wiley & Sons: New York)

Arunyanark A, Jogloy S, Akkasaeng C, Vorasoot N, Kesmala T, Rao RCN, Wright GC, Patanothai A (2008) Chlorophyll stability is an indicator of drought tolerance in peanut. Journal Agronomy & Crop Science 194, 113–125.
Chlorophyll stability is an indicator of drought tolerance in peanut.Crossref | GoogleScholarGoogle Scholar |

Avramova V, Meziane A, Bauer E, Blankenagel S, Eggels S, Gresset S, Grill E, Niculaes C, Ouzunova M, Poppenberger B, Presterl T, Rozhon W, Welcker C, Yang Z, Tardieu F, Schön C-C (2019) Carbon isotope composition, water use efficiency, and drought sensitivity are controlled by a common genomic segment in maize. Theoretical and Applied Genetics 132, 53–63.
Carbon isotope composition, water use efficiency, and drought sensitivity are controlled by a common genomic segment in maize.Crossref | GoogleScholarGoogle Scholar | 30244394PubMed |

Beversdorf WD, Hume DJ, Daonnelly-Vanderloo MJ (1988) Agronomic performance of trianzine-resistant and susceptible reciprocal spring canola hybrids. Crop Science 28, 932–934.
Agronomic performance of trianzine-resistant and susceptible reciprocal spring canola hybrids.Crossref | GoogleScholarGoogle Scholar |

Brown RH, Byrd GT (1997) Transpiration efficiency, specific leaf weight and mineral concentration in peanut and pearl millet. Crop Science 37, 475–480.
Transpiration efficiency, specific leaf weight and mineral concentration in peanut and pearl millet.Crossref | GoogleScholarGoogle Scholar |

Colton B, Potter T (1999) History. In ‘Canola in Australia: the first thirty years’. (Eds PA Salisbury, T Potter, G McDonald, AG Green) pp. 1–4. (The Regional Institute)

Condon AG, Farquhar GD, Richards RA (1990) Genotypic variation in carbon isotope discrimination and transpiration efficiency in wheat. Leaf gas exchange and whole plant studies. Australian Journal of Plant Physiology 17, 9–22.
Genotypic variation in carbon isotope discrimination and transpiration efficiency in wheat. Leaf gas exchange and whole plant studies.Crossref | GoogleScholarGoogle Scholar |

Condon AG, Richards RA (1992) Broad sense heritability and genotypes × environment interaction for carbon isotope discrimination in field-grown wheat. Australian Journal of Agricultural Research 43, 921–934.
Broad sense heritability and genotypes × environment interaction for carbon isotope discrimination in field-grown wheat.Crossref | GoogleScholarGoogle Scholar |

Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2004) Breeding for high water-use efficiency. Journal of Experimental Botany 55, 2447–2460.
Breeding for high water-use efficiency.Crossref | GoogleScholarGoogle Scholar | 15475373PubMed |

Craufurd PQ, Austin RB, Acevedo E, Hall MA (1991) Carbon isotope discrimination and grain yield in barley. Field Crops Research 27, 301–313.
Carbon isotope discrimination and grain yield in barley.Crossref | GoogleScholarGoogle Scholar |

Dingkuhn M, Farquhar GD, De Datta SK, O’Toole JC (1991) Discrimination of 13C among upland rices having different water use efficiencies. Australian Journal of Agricultural Research 42, 1123–1131.
Discrimination of 13C among upland rices having different water use efficiencies.Crossref | GoogleScholarGoogle Scholar |

Ehdaie B, Hall AE, Farquhar GD, Nguyen HT, Waines JG (1991) Water-use efficiency and carbon isotope discrimination in wheat. Crop Science 31, 1282–1288.
Water-use efficiency and carbon isotope discrimination in wheat.Crossref | GoogleScholarGoogle Scholar |

Evans JR (1983) Nitrogen and photosynthesis in the flag leaf of wheat. Plant Physiology 72, 297–302.
Nitrogen and photosynthesis in the flag leaf of wheat.Crossref | GoogleScholarGoogle Scholar | 16662996PubMed |

Evans JR, Sharkey TD, Berry JA, Farquhar GD (1986) Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants. Australian Journal of Plant Physiology 13, 281–292.
Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants.Crossref | GoogleScholarGoogle Scholar |

Fan Z, Stefansson BR, Sernyk JL (1986) Maintainers and restorers for 3 male-sterility-inducing cytoplasms in rape (Brassica napus L.). Canadian Journal of Plant Science 66, 229–234.
Maintainers and restorers for 3 male-sterility-inducing cytoplasms in rape (Brassica napus L.).Crossref | GoogleScholarGoogle Scholar |

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, O’Leary MH, Berry J (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Australian Journal of Plant Physiology 9, 121–137.

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

Fischer RA (1981) Optimizing the use of water and nitrogen through breeding of crops. Plant and Soil 58, 249–278.
Optimizing the use of water and nitrogen through breeding of crops.Crossref | GoogleScholarGoogle Scholar |

Fotovat R, Valizadeh M, Toorchi M (2007) Association between water-use efficiency components and total chlorophyll content (SPAD) in wheat (Triticum aestivum L.) under well-watered and drought stress conditions. Journal of Food Agriculture and Environment 5, 225–227.

Gibberd MR, Walker RR, Blackmore DH, Condon AG (2001) Transpiration efficiency and carbon isotope discrimination of grapevines grown under well-watered conditions in either glasshouse or vineyard. Australian Journal of Grape and Wine Research 7, 110–117.
Transpiration efficiency and carbon isotope discrimination of grapevines grown under well-watered conditions in either glasshouse or vineyard.Crossref | GoogleScholarGoogle Scholar |

Gómez-Campo C (1999) ‘Biology of brassica coenospecies.’ (Elsevier: Amsterdam, The Netherlands)

Hubick K, Farquhar G (1989) Carbon isotope discrimination and the ratio of carbon gained to water lost in barley cultivars. Plant, Cell & Environment 12, 795–804.
Carbon isotope discrimination and the ratio of carbon gained to water lost in barley cultivars.Crossref | GoogleScholarGoogle Scholar |

Hubick KT, Farquhar GD, Shorter R (1986) Correlation between water-use efficiency and carbon isotope discrimination in diverse peanut (Arachis) germplasm. Australian Journal of Plant Physiology 13, 803–816.

Hubick KT, Shorter R, Farquhar GD (1988) Heritability and genotype × environment interactions of carbon isotope discrimination and transpiration efficiency in peanut. Australian Journal of Plant Physiology 15, 799–813.

Hunter MN (1981) Semi-automatic control of soil water in pot culture. Plant and Soil 62, 455–459.
Semi-automatic control of soil water in pot culture.Crossref | GoogleScholarGoogle Scholar |

Impa SM, Nadaradjan S, Boominathan P, Shashidhar G, Bindumadhava H, Sheshshayee MS (2005) Carbon isotope discrimination accurately reflects variability in WUE measured at a whole plant level in rice. Crop Science 45, 2517–2522.
Carbon isotope discrimination accurately reflects variability in WUE measured at a whole plant level in rice.Crossref | GoogleScholarGoogle Scholar |

Johnson RC, Tieszen LL (1994) Variation for water-use efficiency in alfalfa germplasm. Crop Science 34, 452–458.
Variation for water-use efficiency in alfalfa germplasm.Crossref | GoogleScholarGoogle Scholar |

Juenger TE, Mckay JK, Hausmann N, Keurentjes JJB, Sen S, Stowe KA, Dawson TE, Simms EL, Richards RH (2005) Identification and characterization of QTL underlying whole-plant physiology in Arabidopsis thaliana: δ13C, stomatal conductance and transpiration efficiency. Plant, Cell & Environment 28, 697–708.
Identification and characterization of QTL underlying whole-plant physiology in Arabidopsis thaliana: δ13C, stomatal conductance and transpiration efficiency.Crossref | GoogleScholarGoogle Scholar |

Khan HR, Link W, Hocking TJ, Stoddard FL (2007) Evaluation of physiological traits for improving drought tolerance in faba bean (Vicia faba L.). Plant and Soil 292, 205–217.
Evaluation of physiological traits for improving drought tolerance in faba bean (Vicia faba L.).Crossref | GoogleScholarGoogle Scholar |

Knight JD, Livingston NJ, Van Kessel C (1994) Carbon isotope discrimination and water-use efficiency of six crops grown under wet and dryland conditions. Plant, Cell & Environment 17, 173–179.
Carbon isotope discrimination and water-use efficiency of six crops grown under wet and dryland conditions.Crossref | GoogleScholarGoogle Scholar |

Lambrides CJ, Chapman SC, Shorter R (2004) Genetic variation for carbon isotope discrimination in sunflower: association with transpiration efficiency and evidence for cytoplasmic inheritance. Crop Science 44, 1642–1653.
Genetic variation for carbon isotope discrimination in sunflower: association with transpiration efficiency and evidence for cytoplasmic inheritance.Crossref | GoogleScholarGoogle Scholar |

Luckett D, Cowley R (2011) Carbon isotope discrimination in canola: the effect of reduced water availability in a rain-out shelter experiment. In ‘17th Australian research assembly on brassicas’. pp. 5–8. (Australian Research Assembly on Brassicas: Wagga Wagga, NSW, Australia)

Matus A, Slinkard A, Kessel CV (1996) Carbon isotope discrimination and indirect selection for transpiration efficiency at flowering in lentil (Lens culinaris Medikus), spring bread wheat (Triticum aestivum L.) durum wheat (T. turgidum L.), and canola (Brassica napus L.). Euphytica 87, 141–151.
Carbon isotope discrimination and indirect selection for transpiration efficiency at flowering in lentil (Lens culinaris Medikus), spring bread wheat (Triticum aestivum L.) durum wheat (T. turgidum L.), and canola (Brassica napus L.).Crossref | GoogleScholarGoogle Scholar |

Mian MAR, Mailey MA, Ashley DA, Wells R, Carter TE, Parrot WA, Boema HR (1996) Molecular markers associated with water use efficiency and leaf ash in soybean. Crop Science 36, 1252–1257.
Molecular markers associated with water use efficiency and leaf ash in soybean.Crossref | GoogleScholarGoogle Scholar |

Moroni S, Wratten N, Luckett DJ (2009) Carbon isotope discrimination in diverse canola germplasm. In ‘16th Australian research assembly on brassicas’. pp. 1–4. (Australian Research Assembly on Brassicas: Ballarat, Vic., Australia)

Nelson CJ (1988) genetic associations between photosynthetic characteristics and yield – review of the evidence. Plant Physiology and Biochemistry 26, 543–554.

Passioura J (1977) Grain yield, harvest index and water use of wheat. Journal of the Australian Institute of Agricultural Science 43, 117–120.

Pelletier G, Primard C, Vedel F, Chetrit P, Remy R, Rousselle , Renard M (1983) Intergeneric cytoplasmic hybridization in cruciferae by protoplast fusion. Molecular & General Genetics 191, 244–250.
Intergeneric cytoplasmic hybridization in cruciferae by protoplast fusion.Crossref | GoogleScholarGoogle Scholar |

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

Rebetzke GI, Richard RA, Condon AG, Farquhar GD (2006) Inheritance of carbon isotope discrimination in bread wheat (Triticum aestivum L.) Euphytica 150, 97–106.
Inheritance of carbon isotope discrimination in bread wheat (Triticum aestivum L.)Crossref | GoogleScholarGoogle Scholar |

Sayre KD (1995) Carbon isotope discrimination and grain yield for three bread wheat germplasm groups grown at different levels of water stress. Field Crops Research 41, 45–54.
Carbon isotope discrimination and grain yield for three bread wheat germplasm groups grown at different levels of water stress.Crossref | GoogleScholarGoogle Scholar |

Ubierna N, Farquhar GD (2014) Advances in measurements and models of photosynthetic carbon isotope discrimination in C3 plants. Plant, Cell & Environment 37, 1494–1498.
Advances in measurements and models of photosynthetic carbon isotope discrimination in C3 plants.Crossref | GoogleScholarGoogle Scholar |

Virgona JM, Hubick KT, Rawson HM, Farquhar GD, Downes RW (1990) Genotypic variation in transpiration efficiency, carbon-isotope discrimination and carbon allocation during early growth in sunflower. Australian Journal of Plant Physiology 17, 207–214.
Genotypic variation in transpiration efficiency, carbon-isotope discrimination and carbon allocation during early growth in sunflower.Crossref | GoogleScholarGoogle Scholar |

Virgona JM, Farquhar DG (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.

Vos J, Groenwold J (1989) Genetic differences in water-use efficiency, stomatal conductance and carbon isotope fractionation in potato. Potato Research 32, 113–121.
Genetic differences in water-use efficiency, stomatal conductance and carbon isotope fractionation in potato.Crossref | GoogleScholarGoogle Scholar |

Wright GC, Rao RCN, Farquhar GD (1994) Water-use efficiency and carbon-isotope discrimination in peanut under water-deficit conditions. Crop Science 34, 92–97.
Water-use efficiency and carbon-isotope discrimination in peanut under water-deficit conditions.Crossref | GoogleScholarGoogle Scholar |