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

Phenotyping oilseed rape growth-related traits and their responses to water deficit: the disturbing pot size effect

Anaëlle Dambreville A , Mélanie Griolet A , Gaëlle Rolland A , Myriam Dauzat A , Alexis Bédiée A , Crispulo Balsera A , Bertrand Muller A , Denis Vile A and Christine Granier A B
+ Author Affiliations
- Author Affiliations

A INRA, Montpellier SupAgro, UMR759 Laboratoire d’Ecophysiologie des Plantes sous Stress Environnementaux (LEPSE), 2 place Pierre Viala, 34060 Montpellier Cedex 2, France.

B Corresponding author. Email: granier@supagro.inra.fr

Functional Plant Biology 44(1) 35-45 https://doi.org/10.1071/FP16036
Submitted: 27 January 2016  Accepted: 20 May 2016   Published: 4 July 2016

Abstract

Following the recent development of high-throughput phenotyping platforms for plant research, the number of individual plants grown together in a same experiment has raised, sometimes at the expense of pot size. However, root restriction in excessively small pots affects plant growth and carbon partitioning, and may interact with other stresses targeted in these experiments. In work reported here, we investigated the interactive effects of pot size and soil water deficit on multiple growth-related traits from the cellular to the whole-plant scale in oilseed rape (Brassica napus L.). The effects of pot size on responses to water deficit and allometric relationships revealed strong, multilevel interactions between pot size and watering regime. Notably, water deficit increased the root : shoot ratio in large pots, but not in small pots. At the cellular scale, water deficit decreased epidermal leaf cell area in large pots, but not in small pots. These results were consistent with changes in the level of endoreduplication factor in leaf cells. Our study illustrates the disturbing interaction of pot size with water deficit and raises the need to carefully consider this factor in the frame of the current development of high-throughput phenotyping experiments.

Additional keywords: allometry, drought stress, phenotyping platform, plant growth, pot size, stress interactions.


References

Aguirrezabal L, Bouchier-Combaud S, Radziejwoski A, Dauzat M, Cookson SJ, Granier C (2006) Plasticity to soil water deficit in Arabidopsis thaliana: dissection of leaf development into underlying growth dynamic and cellular variables reveals invisible phenotypes. Plant, Cell & Environment 29, 2216–2227.
Plasticity to soil water deficit in Arabidopsis thaliana: dissection of leaf development into underlying growth dynamic and cellular variables reveals invisible phenotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVaiug%3D%3D&md5=b0ed82910f2534ce22b9c6a7626bf6bbCAS |

Bresson J, Vasseur F, Dauzat M, Labadie M, Varoquaux F, Touraine B, Vile D (2014) Interact to survive: Phyllobacterium brassicacearum improves Arabidopsis tolerance to severe water deficit and growth recovery. PLoS One 9, e107607
Interact to survive: Phyllobacterium brassicacearum improves Arabidopsis tolerance to severe water deficit and growth recovery.Crossref | GoogleScholarGoogle Scholar | 25226036PubMed |

Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought – from genes to the whole plant. Functional Plant Biology 30, 239–264.
Understanding plant responses to drought – from genes to the whole plant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtVKlt7o%3D&md5=0c43359463e985e3294c3b6104992db2CAS |

Chen D, Neumann K, Friedel S, Kilian B, Chen M, Altmann T, Klukas C (2014) Dissecting the phenotypic components of crop plant growth and drought responses based on high-throughput image analysis. The Plant Cell 26, 4636–4655.
Dissecting the phenotypic components of crop plant growth and drought responses based on high-throughput image analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXislGmt74%3D&md5=5e48d49e661d43789fe018a849d55f3eCAS | 25501589PubMed |

Cheniclet C, Rong WY, Causse M, Frangne N, Bolling L, Carde JP, Renaudin JP (2005) Cell expansion and endoreduplication show a large genetic variability in pericarp and contribute strongly to tomato fruit growth. Plant Physiology 139, 1984–1994.
Cell expansion and endoreduplication show a large genetic variability in pericarp and contribute strongly to tomato fruit growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlGmsbzM&md5=2b91bf322f8933cfc81613816a0a728aCAS | 16306145PubMed |

Cookson SJ, Van Lijsebettens M, Granier C (2005) Correlation between leaf growth variables suggest intrinsic and early controls of leaf size in Arabidopsis thaliana. Plant, Cell & Environment 28, 1355–1366.
Correlation between leaf growth variables suggest intrinsic and early controls of leaf size in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Dhondt S, Wuyts N, Inzé D (2013) Cell to whole-plant phenotyping: the best is yet to come. Trends in Plant Science 18, 428–439.
Cell to whole-plant phenotyping: the best is yet to come.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXot1Cnu70%3D&md5=a8358176c4f9413b4f477c6a51b588bdCAS | 23706697PubMed |

Endean F, Carlson LW (1975) The effect of rooting volume on the early growth of lodgepole pine seedlings. Canadian Journal of Forest Research 5, 55–60.
The effect of rooting volume on the early growth of lodgepole pine seedlings.Crossref | GoogleScholarGoogle Scholar |

Granier C, Aguirrezabal L, Chenu K, Cookson SJ, Dauzat M, Hamard P, Thioux JJ, Rolland G, Bouchier-Combaud S, Lebaudy A, Muller B, Simonneau T, Tardieu F (2006) PHENOPSIS, an automated platform for reproducible phenotyping of plant responses to soil water deficit in Arabidopsis thaliana permitted the identification of an accession with low sensitivity to soil water deficit. New Phytologist 169, 623–635.
PHENOPSIS, an automated platform for reproducible phenotyping of plant responses to soil water deficit in Arabidopsis thaliana permitted the identification of an accession with low sensitivity to soil water deficit.Crossref | GoogleScholarGoogle Scholar | 16411964PubMed |

Hameed MA, Reid JB, Rowe RN (1987) Root confinement and its effects on the water relations, growth and assimilate partitioning of tomato (Lycopersicon esculentum Mill). Annals of Botany 59, 685–692.

Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regulation 21, 79–102.
Metabolic implications of stress-induced proline accumulation in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1amtLY%3D&md5=8e6720635a192c2ab5f781f72efc9886CAS |

Harris BN, Sadras VO, Tester M (2010) A water-centred framework to assess the effects of salinity on the growth and yield of wheat and barley. Plant and Soil 336, 377–389.
A water-centred framework to assess the effects of salinity on the growth and yield of wheat and barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlWkt7nL&md5=dfe26f91e3f364c2d51e1a0661717df4CAS |

Hauben M, Haesendonckx B, Standaert E, Van Der Kelen K, Azmi A, Akpo H, Van Breusegem F, Guisez Y, Bots M, Lambert B, Laga B, De Block M (2009) Energy use efficiency is characterized by an epigenetic component that can be directed through artificial selection to increase yield. Proceedings of the National Academy of Sciences of the United States of America 106, 20109–20114.
Energy use efficiency is characterized by an epigenetic component that can be directed through artificial selection to increase yield.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFCrsLvL&md5=4b717fafaddf4e90381e4398dd27f07bCAS | 19897729PubMed |

Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80, 1150–1156.
The meta-analysis of response ratios in experimental ecology.Crossref | GoogleScholarGoogle Scholar |

Honsdorf N, March TJ, Berger B, Tester M, Pillen K (2014) High-throughput phenotyping to detect drought tolerance QTL in wild barley introgression lines. PLoS One 9, e97047
High-throughput phenotyping to detect drought tolerance QTL in wild barley introgression lines.Crossref | GoogleScholarGoogle Scholar | 24823485PubMed |

Hummel I, Pantin F, Sulpice R, Piques M, Rolland G, Dauzat M, Christophe A, Pervent M, Bouteillé M, Stitt M, Gibon Y, Muller B (2010) Arabidopsis plants acclimate to water deficit at low cost through changes of carbon usage: an integrated perspective using growth, metabolite, enzyme, and gene expression analysis. Plant Physiology 154, 357–372.
Arabidopsis plants acclimate to water deficit at low cost through changes of carbon usage: an integrated perspective using growth, metabolite, enzyme, and gene expression analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVKrtbrP&md5=2bdca10d1e6ea87f08b2db3a28cfaf40CAS | 20631317PubMed |

Ismail A, Hall A, Bray E (1994) Drought and pot size effects on transpiration efficiency and carbon isotope discrimination of cowpea accessions and hybrids. Functional Plant Biology 21, 23–35.

Junker A, Muraya MM, Weigelt-Fischer K, Arana-Ceballos F, Klukas C, Melchinger AE, Meyer RC, Riewe D, Altmann T (2015) Optimizing experimental procedures for quantitative evaluation of crop plant performance in high throughput phenotyping systems. Frontiers in Plant Science 5, 770
Optimizing experimental procedures for quantitative evaluation of crop plant performance in high throughput phenotyping systems.Crossref | GoogleScholarGoogle Scholar | 25653655PubMed |

Kasai M, Koide K, Ichikawa Y (2012) Effect of pot size on various characteristics related to photosynthetic matter production in soybean plants. International Journal of Agronomy 2012, 1–7.
Effect of pot size on various characteristics related to photosynthetic matter production in soybean plants.Crossref | GoogleScholarGoogle Scholar |

Kawaletz H, Mölder I, Annighöfer P, Terwei A, Zerbe S, Ammer C (2014) Pot experiments with woody species – a review. Forestry 87, 482–491.
Pot experiments with woody species – a review.Crossref | GoogleScholarGoogle Scholar |

Kharkina TG, Ottosen C-O, Rosenqvist E (1999) Effects of root restriction on the growth and physiology of cucumber plants. Physiologia Plantarum 105, 434–441.
Effects of root restriction on the growth and physiology of cucumber plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjsFSisL0%3D&md5=6c1ba11ed8604ea3cb253d313d0a333fCAS |

Körner C (2003) Carbon limitation in trees. Journal of Ecology 91, 4–17.
Carbon limitation in trees.Crossref | GoogleScholarGoogle Scholar |

Lièvre M, Wuyts N, Cookson SJ, Bresson J, Dapp M, Vasseur F, Massonnet C, Tisné S, Bettembourg M, Balsera C, Bédiée A, Bouvery F, Dauzat M, Rolland G, Vile D, Granier C (2013) Phenotyping the kinematics of leaf development in flowering plants: recommendations and pitfalls. Wiley Interdisciplinary Reviews: Developmental Biology 2, 809–821.
Phenotyping the kinematics of leaf development in flowering plants: recommendations and pitfalls.Crossref | GoogleScholarGoogle Scholar | 24123939PubMed |

Longstreth DJ, Nobel PS (1980) Nutrient influences on leaf photosynthesis. Effects of nitrogen, phosphorus, and potassium for Gossypium hirsutum L. Plant Physiology 65, 541–543.
Nutrient influences on leaf photosynthesis. Effects of nitrogen, phosphorus, and potassium for Gossypium hirsutum L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXhvFOjurg%3D&md5=bd270c50109798caf836535eee0c4ab0CAS | 16661231PubMed |

Massonnet C, Tisné S, Radziejwoski A, Vile D, de Veylder L, Dauzat M, Granier C (2011) New insights into the control of endoreduplication: endoreduplication is driven by organ growth in Arabidopsis leaves. Plant Physiology 157, 2044–2055.
New insights into the control of endoreduplication: endoreduplication is driven by organ growth in Arabidopsis leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1ektLzE&md5=0420b3964b2528cbde175c0e4fe3cd27CAS | 22010109PubMed |

Müller T, Lentzsch P, Müller MEH (2012) Carbohydrate dynamics in leaves of rapeseed (Brassica napus) under drought. Journal Agronomy & Crop Science 198, 207–217.
Carbohydrate dynamics in leaves of rapeseed (Brassica napus) under drought.Crossref | GoogleScholarGoogle Scholar |

Mutsaers HJW (1983) Leaf growth in cotton (Gossypium hirsutum L.) 2. The influence of temperature, light, water stress and root restriction on the growth and initiation of leaves. Annals of Botany 51, 521–529.

Nagel KA, Putz A, Gilmer F, Heinz K, Fischbach A, Pfeifer J, Faget M, Blossfeld S, Ernst M, Dimaki C, Kastenholz B, Kleinert A-K, Galinski A, Scharr H, Fiorani F, Schurr U (2012) GROWSCREEN-Rhizo is a novel phenotyping robot enabling simultaneous measurements of root and shoot growth for plants grown in soil-filled rhizotrons. Functional Plant Biology 39, 891–904.
GROWSCREEN-Rhizo is a novel phenotyping robot enabling simultaneous measurements of root and shoot growth for plants grown in soil-filled rhizotrons.Crossref | GoogleScholarGoogle Scholar |

NeSmith DS, Bridges DC, Barbour JC (1992) Bell pepper responses to root restriction. Journal of Plant Nutrition 15, 2763–2776.
Bell pepper responses to root restriction.Crossref | GoogleScholarGoogle Scholar |

Omidi H (2010) Changes of proline content and activity of antioxidative enzymes in two canola genotype under drought stress. American Journal of Plant Physiology 5, 338–349.
Changes of proline content and activity of antioxidative enzymes in two canola genotype under drought stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFCnsrvN&md5=24452110811c4c569107148d7bbc1a7cCAS |

Passioura JB (2006) The perils of pot experiments. Functional Plant Biology 33, 1075–1079.
The perils of pot experiments.Crossref | GoogleScholarGoogle Scholar |

Poorter H, Niinemets U, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytologist 182, 565–588.
Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis.Crossref | GoogleScholarGoogle Scholar | 19434804PubMed |

Poorter H, Bühler J, van Dusschoten D, Climent J, Postma JA (2012a) Pot size matters: a meta-analysis of the effects of rooting volume on plant growth. Functional Plant Biology 39, 839–850.
Pot size matters: a meta-analysis of the effects of rooting volume on plant growth.Crossref | GoogleScholarGoogle Scholar |

Poorter H, Fiorani F, Stitt M, et al (2012b) The art of growing plants for experimental purposes: a practical guide for the plant biologist. Functional Plant Biology 39, 821–838.
The art of growing plants for experimental purposes: a practical guide for the plant biologist.Crossref | GoogleScholarGoogle Scholar |

Ray JD, Sinclair TR (1998) The effect of pot size on growth and transpiration of maize and soybean during water deficit stress. Journal of Experimental Botany 49, 1381–1386.
The effect of pot size on growth and transpiration of maize and soybean during water deficit stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlsVOkt78%3D&md5=e323c92041be065cdf38527d0d3f08f4CAS |

Richards D, Rowe RN (1977) Effects of root restriction, root pruning and 6-benzylaminopurine on the growth of peach seedlings. Annals of Botany 41, 729–740.

Ronchi CP, DaMatta FM, Batista KD, Moraes GABK, Loureiro ME, Ducatti C (2006) Growth and photosynthetic down-regulation in Coffea arabica in response to restricted root volume. Functional Plant Biology 33, 1013–1023.
Growth and photosynthetic down-regulation in Coffea arabica in response to restricted root volume.Crossref | GoogleScholarGoogle Scholar |

Sadok W, Naudin P, Boussuge B, Muller B, Welcker C, Tardieu F (2007) Leaf growth rate per unit thermal time follows QTL-dependent daily patterns in hundreds of maize lines under naturally fluctuating conditions. Plant, Cell & Environment 30, 135–146.
Leaf growth rate per unit thermal time follows QTL-dependent daily patterns in hundreds of maize lines under naturally fluctuating conditions.Crossref | GoogleScholarGoogle Scholar |

Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675.
NIH Image to ImageJ: 25 years of image analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVKntb7P&md5=71447d5ca15dc8993428944031d55206CAS | 22930834PubMed |

Schwarz D, Thompson AJ, Kläring H-P (2014) Guidelines to use tomato in experiments with a controlled environment. Frontiers in Plant Science 5, 625
Guidelines to use tomato in experiments with a controlled environment.Crossref | GoogleScholarGoogle Scholar | 25477888PubMed |

Shi K, Ding X-T, Dong D-K, Zhou Y-H, Yu J-Q (2008) Root restriction-induced limitation to photosynthesis in tomato (Lycopersicon esculentum Mill.) leaves. Scientia Horticulturae 117, 197–202.
Root restriction-induced limitation to photosynthesis in tomato (Lycopersicon esculentum Mill.) leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotlOjuro%3D&md5=e7649756bd8e03bcdb1fa5dcee3de899CAS |

Skirycz A, Vandenbroucke K, Clauw P, Maleux K, De Meyer B, Dhondt S, Pucci A, Gonzalez N, Hoeberichts F, Tognetti VB, Galbiati M, Tonelli C, Van Breusegem F, Vuylsteke M, Inzé D (2011) Survival and growth of Arabidopsis plants given limited water are not equal. Nature Biotechnology 29, 212–214.
Survival and growth of Arabidopsis plants given limited water are not equal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXivFWktr8%3D&md5=a8c76f58aa47419f9e7d391a75d6894eCAS | 21390020PubMed |

Tardieu F, Granier C, Muller B (1999) Modelling leaf expansion in a fluctuating environment: are changes in specific leaf area a consequence of changes in expansion rate? New Phytologist 143, 33–43.
Modelling leaf expansion in a fluctuating environment: are changes in specific leaf area a consequence of changes in expansion rate?Crossref | GoogleScholarGoogle Scholar |

Tardieu F, Granier C, Muller B (2011) Water deficit and growth. Co-ordinating processes without an orchestrator? Current Opinion in Plant Biology 14, 283–289.
Water deficit and growth. Co-ordinating processes without an orchestrator?Crossref | GoogleScholarGoogle Scholar | 21388861PubMed |

Ternesi M, Andrade AP, Jorrin J, Benlloch M (1994) Root–shoot signalling in sunflower plants with confined root systems. Plant and Soil 166, 31–36.
Root–shoot signalling in sunflower plants with confined root systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjsFKmurY%3D&md5=759e6a6894a5445e4414ff64fba1422aCAS |

Thomas RB, Strain BR (1991) Root restriction as a factor in photosynthetic acclimation of cotton seedlings grown in elevated carbon dioxide. Plant Physiology 96, 627–634.
Root restriction as a factor in photosynthetic acclimation of cotton seedlings grown in elevated carbon dioxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXksVKgsrc%3D&md5=d38d80033859310f96177bf5cbc742bdCAS | 16668232PubMed |

Tisné S, Serrand Y, Bach L, Gilbault E, Ben Ameur R, Balasse H, Voisin R, Bouchez D, Durand-Tardif M, Guerche P, Chareyron G, Da Rugna J, Camilleri C, Loudet O (2013) Phenoscope: an automated large-scale phenotyping platform offering high spatial homogeneity. The Plant Journal 74, 534–544.
Phenoscope: an automated large-scale phenotyping platform offering high spatial homogeneity.Crossref | GoogleScholarGoogle Scholar | 23452317PubMed |

Troll W, Lindsley J (1955) A photometric method for the determination of proline. Journal of Biological Chemistry 215, 655–660.

Trotel P, Bouchereau A, Niogret MF, Larher F (1996) The fate of osmo-accumulated proline in leaf discs of rape (Brassica napus L.) incubated in a medium of low osmolarity. Plant Science 118, 31–45.
The fate of osmo-accumulated proline in leaf discs of rape (Brassica napus L.) incubated in a medium of low osmolarity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjsFOlsbk%3D&md5=6beb0e8fe9390ce9531a95fcc9e187e3CAS |

Vile D, Pervent M, Belluau M, Vasseur F, Bresson J, Muller B, Granier C, Simonneau T (2012) Arabidopsis growth under prolonged high temperature and water deficit: independent or interactive effects? Plant, Cell & Environment 35, 702–718.
Arabidopsis growth under prolonged high temperature and water deficit: independent or interactive effects?Crossref | GoogleScholarGoogle Scholar |

Whitfield CP, Davison AW, Ashenden TW (1996) Interactive effects of ozone and soil volume on Plantago major. New Phytologist 134, 287–294.
Interactive effects of ozone and soil volume on Plantago major.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xnt1Kgs74%3D&md5=c9445d44c8a76f79866d6a7927d9bdafCAS |

Wu Y, Huang M, Warrington DN (2011) Growth and transpiration of maize and winter wheat in response to water deficits in pots and plots. Environmental and Experimental Botany 71, 65–71.
Growth and transpiration of maize and winter wheat in response to water deficits in pots and plots.Crossref | GoogleScholarGoogle Scholar |

Yeh DM, Chiang HH (2001) Growth and flower initiation in hydrangea as affected by root restriction and defoliation. Scientia Horticulturae 91, 123–132.
Growth and flower initiation in hydrangea as affected by root restriction and defoliation.Crossref | GoogleScholarGoogle Scholar |

Zaharah SS, Razi IM (2009) Growth, stomata aperture, biochemical changes and branch anatomy in mango (Mangifera indica) cv. Chokanan in response to root restriction and water stress. Scientia Horticulturae 123, 58–67.
Growth, stomata aperture, biochemical changes and branch anatomy in mango (Mangifera indica) cv. Chokanan in response to root restriction and water stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1ajurjF&md5=47bd61346244dad263f32ab2a1098ebeCAS |