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

Stress-induced changes in carbon allocation among metabolite pools influence isotope-based predictions of water use efficiency in Phaseolus vulgaris

Erin Lockhart A , Birgit Wild B C , Andreas Richter C , Kevin Simonin A D and Andrew Merchant A E
+ Author Affiliations
- Author Affiliations

A Department of Environmental Sciences, Faculty of Agriculture and Environment, The University of Sydney, Sydney, NSW 2006, Australia.

B Department of Earth Sciences, University of Gothenburg, Gothenburg 40530, Sweden.

C Department of Microbiology and Ecosystem Science, University of Vienna, Vienna 1090, Austria.

D Department of Biology, San Francisco State University, San Francisco, CA 94132, USA.

E Corresponding author. Email: andrew.merchant@sydney.edu.au

Functional Plant Biology 43(12) 1149-1158 https://doi.org/10.1071/FP16022
Submitted: 18 January 2016  Accepted: 31 July 2016   Published: 5 September 2016

Abstract

Understanding how major food crops respond to environmental stress will expand our capacity to improve food production with growing populations and a changing climate. This study uses chemical and physiological adaptations to heat, water deficit and elevated light stresses in Phaseolus vulgaris L. to identify changes in carbon (C) allocation that, combined with post-photosynthetic fractionation of C isotopes, influences water use efficiency (WUE) predictions. The chemical stress response was explored through changes in C allocation to the carbohydrate and cyclitol pools using GC–triple quadrupole MS. Carbon allocation to the sucrose pool fluctuated significantly among treatments, and the putative osmolytes and osmoprotectants (myo-inositol and d-ononitol) accumulated under stress. Significant osmotic adjustment (P < 0.05), quantified via pressure–volume curve analysis, was detected between control and stress treatments, although this was not attributable to active accumulation of the metabolites. Compound-specific 13C isotope abundance was measured using liquid chromatography isotope ratio MS to predict intrinsic WUE. In contrast to other metabolites measured, the δ13C of the sucrose pool fluctuated according to treatment and was proportional to predicted values based upon modelled Δ13C from gas exchange data. The results suggest that the accuracy and precision of predicting WUE may be enhanced by compound-specific analysis of Δ13C and that changes in the allocation of C among metabolite pools may influence WUE predictions based upon analysis of total soluble C. Overall, the plants appeared to use a range of mechanisms to cope with adverse conditions that could be utilised to improve plant breeding and management strategies.

Additional keywords: abiotic stress, carbohydrate, common bean, d-ononitol, myo-inositol.


References

Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynthesis Research 98, 541–550.
Heat stress: an overview of molecular responses in photosynthesis.CrossRef | 1:CAS:528:DC%2BD1cXhsVOgt7bF&md5=560030f7bc5ded60e19a2bed3b544124CAS | 18649006PubMed |

Barbour MM, Warren CR, Farquhar GD, Forrester G, Brown H (2010) Variability in mesophyll conductance between barley genotypes, and effects on transpiration efficiency and carbon isotope discrimination. Plant, Cell & Environment 33, 1176–1185.

Bohnert HJ, Jensen RG (1996) Strategies for engineering water-stress tolerance in plants. Trends in Biotechnology 14, 89–97.
Strategies for engineering water-stress tolerance in plants.CrossRef | 1:CAS:528:DyaK28XhsleqtLo%3D&md5=75432648ea78c8181739c8fd27bf6cf7CAS |

Bohnert HJ, Shen B (1998) Transformation and compatible solutes. Scientia Horticulturae 78, 237–260.
Transformation and compatible solutes.CrossRef |

Cavalieri A, Merchant A, van Volkenburgh E (2011) Why not beans? Foreword. Functional Plant Biology 38, iii–vi.
Why not beans? Foreword.CrossRef |

Cernusak LA, Tcherkez G, Keitel C, Cornwell WK, Santiago LS, Knohl A, Barbour MM, Williams DG, Reich PB, Ellsworth DS, Dawson TE, Griffiths HG, Farquhar GD, Wright IJ (2009) Why are non-photosynthetic tissues generally 13C enriched compared with leaves in C3 plants? Review and synthesis of current hypotheses. Functional Plant Biology 36, 199–213.
Why are non-photosynthetic tissues generally 13C enriched compared with leaves in C3 plants? Review and synthesis of current hypotheses.CrossRef | 1:CAS:528:DC%2BD1MXisFSqtbc%3D&md5=afa3456bee4446eef2fd2bdd9926d9e3CAS |

Cowan IR (1978) Stomatal behaviour and environment. In ‘Advances in botanical research. Vol. 4’. (Eds RD Preston, HW Woolhouse.) pp. 117–228. (Academic Press: London)

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.
Isotopic composition of plant carbon correlates with water use efficiency of wheat genotypes.CrossRef | 1:CAS:528:DyaL2MXhtFSju7w%3D&md5=3c3a8b38a8403055e87bdf9712593c16CAS |

Farquhar GD, Oleary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Australian Journal of Plant Physiology 9, 121–137.
On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves.CrossRef | 1:CAS:528:DyaL38XhsF2ms70%3D&md5=4d02e48ff2b5de0ba0d3bbf77b58f767CAS |

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 | 1:CAS:528:DyaL1MXktlKmu70%3D&md5=eedbc63279977192077254b365f54f69CAS |

Ford CW (1984) Accumulation of low molecular weight solutes in water-stressed tropical legumes. Phytochemistry 23, 1007–1015.
Accumulation of low molecular weight solutes in water-stressed tropical legumes.CrossRef | 1:CAS:528:DyaL2cXls1OisL4%3D&md5=d1dd5dddb0e24c479f20823ed2497379CAS |

Guo CX, Oosterhuis DM (1995) Pinitol occurrence in soybean plants as affected by temperature and plant growth regulators. Journal of Experimental Botany 46, 249–253.
Pinitol occurrence in soybean plants as affected by temperature and plant growth regulators.CrossRef | 1:CAS:528:DyaK2MXktVOrsLY%3D&md5=7d69f315d77786aadbaae6f65d23b096CAS |

Hare PD, Cress WA, Van Staden J (1998a) Dissecting the roles of osmolyte accumulation during stress. Plant, Cell & Environment 21, 535–553.
Dissecting the roles of osmolyte accumulation during stress.CrossRef | 1:CAS:528:DyaK1cXltl2hu7s%3D&md5=245f3a011877c12f1e770d98ba009dbeCAS |

Hare PD, Cress WA, Van Staden J (1998b) Dissecting the roles of osmolyte accumulation during stress. Plant, Cell & Environment 21, 535–553.
Dissecting the roles of osmolyte accumulation during stress.CrossRef | 1:CAS:528:DyaK1cXltl2hu7s%3D&md5=245f3a011877c12f1e770d98ba009dbeCAS |

Hettmann E, Brand WA, Gleixner G (2007) Improved isotope ratio measurement performance in liquid chromatography/isotope ratio mass spectrometry by removing excess oxygen. Rapid Communications in Mass Spectrometry 21, 4135–4141.
Improved isotope ratio measurement performance in liquid chromatography/isotope ratio mass spectrometry by removing excess oxygen.CrossRef | 1:CAS:528:DC%2BD1cXot1ym&md5=cacba175f4136108988c832ce1835acdCAS | 18041012PubMed |

Krummen M, Hilkert AW, Juchelka D, Duhr A, Schluter HJ, Pesch R (2004) A new concept for isotope ratio monitoring liquid chromatography/mass spectrometry. Rapid Communications in Mass Spectrometry 18, 2260–2266.
A new concept for isotope ratio monitoring liquid chromatography/mass spectrometry.CrossRef | 1:CAS:528:DC%2BD2cXot1CmsLk%3D&md5=56bc8b02a610a61274d45b68401788ddCAS | 15384146PubMed |

Laurie S, Stewart GR (1990) The effects of compatible solutes on the heat-stability of glutamine-synthetase from chickpeas grown under different nitrogen and temperature regimes. Journal of Experimental Botany 41, 1415–1422.
The effects of compatible solutes on the heat-stability of glutamine-synthetase from chickpeas grown under different nitrogen and temperature regimes.CrossRef | 1:CAS:528:DyaK3MXpslWntg%3D%3D&md5=ddb9dac85d578366126b901d20617cb0CAS |

Merchant A, Richter AA (2011) Polyols as biomarkers and bioindicators for 21st century plant breeding. Functional Plant Biology 38, 934–940.
Polyols as biomarkers and bioindicators for 21st century plant breeding.CrossRef | 1:CAS:528:DC%2BC3MXhsFKktLvL&md5=dac3efb6035276807e8a4a156e394865CAS |

Merchant A, Richter A, Popp M, Adams M (2006) Targeted metabolite profiling provides a functional link among eucalypt taxonomy, physiology and evolution. Phytochemistry 67, 402–408.
Targeted metabolite profiling provides a functional link among eucalypt taxonomy, physiology and evolution.CrossRef | 1:CAS:528:DC%2BD28XnvVahug%3D%3D&md5=0f85a3c947d35fd21c434c0af09c5567CAS | 16426650PubMed |

Merchant A, Ladiges PY, Adams MA (2007) Quercitol links the physiology, taxonomy and evolution of 279 eucalypt species. Global Ecology and Biogeography 16, 810–819.
Quercitol links the physiology, taxonomy and evolution of 279 eucalypt species.CrossRef |

Merchant A, Peuke AD, Keitel C, Macfarlane C, Warren C, Adams MA (2010) Phloem sap and leaf δ13C, carbohydrates and amino acid concentrations in Eucalyptus globulus change systematically according to flooding and water deficit treatment. Journal of Experimental Botany 61, 1785–1793.
Phloem sap and leaf δ13C, carbohydrates and amino acid concentrations in Eucalyptus globulus change systematically according to flooding and water deficit treatment.CrossRef | 1:CAS:528:DC%2BC3cXkvVOhurk%3D&md5=846ed127515ab455826f6e969c8bd832CAS | 20211969PubMed |

Merchant A, Wild B, Richter A, Bellot S, Adams MA, Dreyer E (2011) Compound-specific differences in 13C of soluble carbohydrates in leaves and phloem of 6-month-old Eucalyptus globulus (Labill). Plant, Cell & Environment 34, 1599–1608.
Compound-specific differences in 13C of soluble carbohydrates in leaves and phloem of 6-month-old Eucalyptus globulus (Labill).CrossRef | 1:CAS:528:DC%2BC3MXht1yms7nF&md5=f5205e95f39c0fb5ab454bf089ea8a79CAS |

Orthen B, Popp M, Smirnoff N (1994) Hydroxyl radical scavenging properties of cyclitols. Proceedings of the Royal Society of Edinburgh. Section B, Biological Sciences 102, 269–272.

Pattanagul W, Madore MA (1999) Water deficit effects on raffinose family oligosaccharide metabolism in coleus Plant Physiology 121, 987–993.
Water deficit effects on raffinose family oligosaccharide metabolism in coleusCrossRef | 1:CAS:528:DyaK1MXns12ntbY%3D&md5=a7dd6bbfb48f9d5713d04f0c78f758fcCAS | 10557248PubMed |

Paul MJ, Cockburn W (1989) Pinitol, a compatible solute in Mesembryanthemum crystallinum L. Journal of Experimental Botany 40, 1093–1098.
Pinitol, a compatible solute in Mesembryanthemum crystallinum L.CrossRef | 1:CAS:528:DyaK3cXjtlCisA%3D%3D&md5=de00fc727d283e3ce05edf4203b03826CAS |

Popp M, Lied W, Meyer AJ, Richter A, Schiller P, Schwitte H (1996) Sample preservation for determination of organic compounds: microwave vs freeze drying. Journal of Experimental Botany 47, 1469–1473.
Sample preservation for determination of organic compounds: microwave vs freeze drying.CrossRef | 1:CAS:528:DyaK28XntVamu7w%3D&md5=35222d53123c49fc7e270936cb6abd9aCAS |

Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. Journal of Plant Physiology 161, 1189–1202.
Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants.CrossRef | 1:CAS:528:DC%2BD2MXhvFegtA%3D%3D&md5=9ba62220d732d9c05421e064f236b7c0CAS |

Reynolds-Henne CE, Langenegger A, Mani J, Schenk N, Zumsteg A, Feller U (2010) Interactions between temperature, drought and stomatal opening in legumes. Environmental and Experimental Botany 68, 37–43.
Interactions between temperature, drought and stomatal opening in legumes.CrossRef |

Sheveleva E, Chmara W, Bohnert HJ, Jensen RG (1997) Increased salt and drought tolerance by d-ononitol production in transgenic Nicotiana tabacum L. Plant Physiology 115, 1211–1219.

Shrestha R, Turner NC, Siddique KHM, Turner DW (2006) Physiological and seed yield responses to water deficits among lentil genotypes from diverse origins. Australian Journal of Agricultural Research 57, 903–915.
Physiological and seed yield responses to water deficits among lentil genotypes from diverse origins.CrossRef |

Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant, Cell & Environment 30, 1126–1149.
Coordination of carbon supply and plant growth.CrossRef | 1:CAS:528:DC%2BD2sXhtVeiurrJ&md5=02da595184420a30d728b8dbb8ca5412CAS |

Stitt M, Lunn J, Usadel B (2010) Arabidopsis and primary photosynthetic metabolism – more than the icing on the cake. The Plant Journal 61, 1067–1091.
Arabidopsis and primary photosynthetic metabolism – more than the icing on the cake.CrossRef | 1:CAS:528:DC%2BC3cXkvFKntLw%3D&md5=ca1401625506522c2f8a6973dd511858CAS | 20409279PubMed |

Streeter JG, Lohnes DG, Fioritto RJ (2001) Patterns of pinitol accumulation in soybean plants and relationships to drought tolerance. Plant, Cell & Environment 24, 429–438.
Patterns of pinitol accumulation in soybean plants and relationships to drought tolerance.CrossRef | 1:CAS:528:DC%2BD3MXjtFyjtLg%3D&md5=f76dac094b593c5a5da8de7d62945074CAS |

Tardieu F, Simonneau T (1998) Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours. Journal of Experimental Botany 49, 419–432.
Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours.CrossRef |

Turner NC, Long MJ (1980) Errors arising from rapid water-loss in the measurement of leaf water potential by the pressure chamber technique. Australian Journal of Plant Physiology 7, 527–537.
Errors arising from rapid water-loss in the measurement of leaf water potential by the pressure chamber technique.CrossRef |

Vernon DM, Tarczynski MC, Jensen RG, Bohnert HJ (1993) Cyclitol production in transgenic tobacco. The Plant Journal 4, 199–205.
Cyclitol production in transgenic tobacco.CrossRef | 1:CAS:528:DyaK2cXhvVOhtrg%3D&md5=e47c6c5229a564ad6ea6c5612c22d5caCAS |

Warren CR, Aranda I, Cano FJ (2011) Responses to water stress of gas exchange and metabolites in Eucalyptus and Acacia spp. Plant, Cell & Environment 34, 1609–1629.
Responses to water stress of gas exchange and metabolites in Eucalyptus and Acacia spp.CrossRef | 1:CAS:528:DC%2BC3MXhtlarurjK&md5=a6cb0fa0fe45c0b1df92f6673a53aa47CAS |

Wild B, Wanek W, Postl W, Richter A (2010) Contribution of carbon fixed by Rubisco and PEPC to phloem export in the Crassulacean acid metabolism plant Kalanchoe daigremontiana. Journal of Experimental Botany 61, 1375–1383.
Contribution of carbon fixed by Rubisco and PEPC to phloem export in the Crassulacean acid metabolism plant Kalanchoe daigremontiana.CrossRef | 1:CAS:528:DC%2BC3cXjt1Kgur0%3D&md5=65f57d8104d4796740145832b2b903c1CAS | 20159885PubMed |

Xu BC, Deng XP, Zhang SQ, Shan L (2010) Biomass partition, leaf gas exchange and water relations of alfalfa and milkvetch seedlings in response to soil drying. Photosynthetica 48, 481–487.
Biomass partition, leaf gas exchange and water relations of alfalfa and milkvetch seedlings in response to soil drying.CrossRef |



Rent Article (via Deepdyve) Export Citation