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

Relationships between biomass allocation, axis organogenesis and organ expansion under shading and water deficit conditions in grapevine

Benoît Pallas A and Angélique Christophe B C D
+ Author Affiliations
- Author Affiliations

A INRA, UMR AGAP, Avenue d’Agropolis, F-34398 Montpellier Cedex 5, France.

B INRA, UMR759 LEPSE, F-34060 Montpellier, France.

C Montpellier SupAgro, UMR759 LEPSE, F-34060 Montpellier, France.

D Corresponding author. Email: christop@supagro.inra.fr

Functional Plant Biology 42(12) 1116-1128 https://doi.org/10.1071/FP15168
Submitted: 17 June 2015  Accepted: 9 September 2015   Published: 23 October 2015

Abstract

The relationships between whole-plant growth and morphogenetic processes under abiotic stresses are still partly unknown. Whole-plant biomass growth can be decreased by many abiotic stresses, including water deficit and shading. Two experiments were performed on potted plants of one grapevine cultivar (Vitis vinifera L. cv. Syrah) subjected to watering and shading treatments. Under water stress, plants reduced their primary and secondary axis leaf production rate, whereas secondary axis budburst was relatively unaffected. Individual leaf area was reduced and a strong decrease in leaf expansion rate was observed. Under shading, primary axis organogenesis was maintained, both secondary axis budburst rate and phytomer appearance rate were decreased, and individual leaf area slightly increased. Specific leaf area did not change under soil water deficit, whereas it increased under shading. These results confirm the existence of dynamic changes in organ sink strength and biomass allocation patterns to favour plant leaf area growth under shading, and to reduce plant leaf area and water losses by transpiration under water stress. From a modelling point of view, this study shows that functional structural models based on a C balance are not fully relevant for simulating plant growth under abiotic constraints if they do not include non-trophic relationships (hormonal signalling or plant hydraulic properties) that modify organ sink strength according to abiotic constraints.

Additional keywords: branching, leaf area, Vitis vinifera L.


References

Aguirrezabal L, Bouchier-Combaud S, Radziejwoski A, Dauzat M, Cookson S, 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=2d08a5b444f9bf756cd6e1c4cbef52aaCAS |

Ben Haj Salah H, Tardieu F (1996) Quantitative analysis of the combined effects of temperature, evaporative demand and light on leaf elongation rate in well watered field and laboratory grown maize plants. Journal of Experimental Botany 47, 1689–1698.
Quantitative analysis of the combined effects of temperature, evaporative demand and light on leaf elongation rate in well watered field and laboratory grown maize plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjsFCrtA%3D%3D&md5=96fd94c1f135820cb039fac9f02c1ee6CAS |

Brouwer R (1963) Some aspects of the equilibrium between overground and underground plant parts. Mededeling – Instituut voor Biologisch en Scheikundig Onderzoek van Landbouwgewassen 213, 31–39.

Brouwer R (1983) Functional equilibrium: sense or nonsense? Netherlands Journal of Agricultural Science 31, 335–342.

Casadebaig P, Debaeke P, Lecoeur J (2008) Thresholds for leaf expansion and transpiration response to soil water deficit in a range of sunflower genotypes. European Journal of Agronomy 28, 646–654.
Thresholds for leaf expansion and transpiration response to soil water deficit in a range of sunflower genotypes.Crossref | GoogleScholarGoogle Scholar |

Champagnol F (1984). ‘Éléments de physiologie de la vigne et de viticulture générale.’ (Imprimerie Déhan: Montpellier)

Chaves MM, Santos TP, Souza CR, Ortuno MF, Rodrigues ML, Lopes CM, Maroco JP, Pereira JS (2007) Deficit irrigation in grapevine improves water-use efficiency while controlling vigour and production quality. Annals of Applied Biology 150, 237–252.
Deficit irrigation in grapevine improves water-use efficiency while controlling vigour and production quality.Crossref | GoogleScholarGoogle Scholar |

Christophe A, Moulia B, Varlet-Grancher C (2006) Quantitative contributions of blue light and PAR to the photocontrol of plant morphogenesis in Trifolium repens (L.). Journal of Experimental Botany 57, 2379–2390.
Quantitative contributions of blue light and PAR to the photocontrol of plant morphogenesis in Trifolium repens (L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnvF2lsr0%3D&md5=4e4261a89173b54f85187d1b4a210629CAS | 16798853PubMed |

Cookson S, Granier C (2006) A dynamic analysis of the shade-induced plasticity in Arabidopsis thaliana rosette leaf development reveals new components of the shade-adaptative response. Annals of Botany 97, 443–452.
A dynamic analysis of the shade-induced plasticity in Arabidopsis thaliana rosette leaf development reveals new components of the shade-adaptative response.Crossref | GoogleScholarGoogle Scholar | 16371443PubMed |

Coombe BG (1995) Adoption of a system for identifying grapevine growth stages. Australian Journal of Grape and Wine Research 1, 104–110.
Adoption of a system for identifying grapevine growth stages.Crossref | GoogleScholarGoogle Scholar |

Egea G, Verhoef A, Vidale PL (2011) Towards an improved and more flexible representation of water stress in coupled photosynthesis–stomatal models. Agricultural and Forest Meteorology 151, 1370–1384.
Towards an improved and more flexible representation of water stress in coupled photosynthesis–stomatal models.Crossref | GoogleScholarGoogle Scholar |

Gautier H, Varlet-Grancher C, Baudry N (1998) Comparison of horizontal spread of white clover (Trifolium repens L.) grown under two artificial light sources differing in their content of blue light. Annals of Botany 82, 41–48.
Comparison of horizontal spread of white clover (Trifolium repens L.) grown under two artificial light sources differing in their content of blue light.Crossref | GoogleScholarGoogle Scholar |

Grechi I, Vivin P, Hilbert G, Milin S, Robert T, Gaudillère JP (2007) Effect of light and nitrogen supply on internal C : N balance and control of root-to-shoot biomass allocation in grapevine. Environmental and Experimental Botany 59, 139–149.
Effect of light and nitrogen supply on internal C : N balance and control of root-to-shoot biomass allocation in grapevine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1Cqtb%2FI&md5=d829e30db1dcaec1a2fce9672ffeeb8aCAS |

Grime J (1981). Plant strategies in shade. In: ‘Plant strategies in shade’(Ed H Smith H) p. 159–186. (London: Academic Press)

Guilioni L, Wéry J, Lecoeur J (2003) High temperature and water deficit may reduce seed number in field pea purely by decreasing plant growth rate. Functional Plant Biology 30, 1151–1164.
High temperature and water deficit may reduce seed number in field pea purely by decreasing plant growth rate.Crossref | GoogleScholarGoogle Scholar |

Holzapfel BP, Smith JP, Field S, Hardie WJ (2010) Dynamics of carbohydrate reserves in cultivated grapevines. Horticultural Reviews 37, 143–211.

Hsiao TC, Acevedo E (1974) Plant response to water deficits, water use efficiency, and drought resistance. Agricultural Meteorology 14, 59–84.
Plant response to water deficits, water use efficiency, and drought resistance.Crossref | GoogleScholarGoogle Scholar |

Jacquinet A, Simon JL (1971) Contribution à l’étude de la croissance des rameaux de vigne. Revue Suisse de Viticulture, d’Arboriculture et d’Horticulture 3, 131–135.

James SA, Bell DT (2000) Influence of light availability on leaf structure and growth of two Eucalyptus globulus ssp. globulus provenances. Tree Physiology 20, 1007–1018.
Influence of light availability on leaf structure and growth of two Eucalyptus globulus ssp. globulus provenances.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MzjvFKnsA%3D%3D&md5=3f2e35bc0d5c10abfdd4e0bc47d27063CAS | 11305455PubMed |

Kang M, Yang L, Zhang B, de Reffye P (2011) Correlation between dynamic tomato fruit-set and source–sink ratio: a common relationship for different plant densities and seasons. Annals of Botany 107, 805–815.
Correlation between dynamic tomato fruit-set and source–sink ratio: a common relationship for different plant densities and seasons.Crossref | GoogleScholarGoogle Scholar | 21183453PubMed |

Lafarge T, Seassau C, Martin M, Bueno C, Clément-Vidal A, Schreck E, Luquet D (2010) Regulation and recovery of sink strength in rice plants grown under changes in light intensity. Functional Plant Biology 37, 413–428.
Regulation and recovery of sink strength in rice plants grown under changes in light intensity.Crossref | GoogleScholarGoogle Scholar |

Lebon E, Pellegrino A, Tardieu F, Lecoeur J (2004) Shoot development in grapevine (Vitis vinifera L.) is affected by the modular branching pattern of the stem and intra- inter-shoot trophic competition. Annals of Botany 46, 1093–1101.

Lebon E, Pellegrino A, Louarn G, Lecoeur J (2006) Branch development controls leaf area dynamics in grapevine (Vitis vinifera) growing in drying soil. Annals of Botany 98, 175–185.
Branch development controls leaf area dynamics in grapevine (Vitis vinifera) growing in drying soil.Crossref | GoogleScholarGoogle Scholar | 16679414PubMed |

Louarn G, Guédon Y, Lecoeur J, Lebon E (2007) Quantitative analysis of the phenotypic variability of shoot architecture in two grapevine cultivars (Vitis vinifera L.). Annals of Botany 99, 425–437.
Quantitative analysis of the phenotypic variability of shoot architecture in two grapevine cultivars (Vitis vinifera L.).Crossref | GoogleScholarGoogle Scholar | 17204533PubMed |

Luquet D, Dingkuhn M, Kim H, Tambour L, Clément-Vidal A (2006) EcoMeristem: a model of morphogenesis and competition among sinks in rice. 1. Concept, validation and sensitivity analysis. Functional Plant Biology 33, 309–323.
EcoMeristem: a model of morphogenesis and competition among sinks in rice. 1. Concept, validation and sensitivity analysis.Crossref | GoogleScholarGoogle Scholar |

Marguerit E, Brendel O, Lebon E, Van Leeuwen C, Ollat N (2012) Rootstock control of scion transpiration and its acclimation to water deficit are controlled by different genes. New Phytologist 194, 416–429.
Rootstock control of scion transpiration and its acclimation to water deficit are controlled by different genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmsFChsbw%3D&md5=52f7b3cb436733b7e1c249316bfe7c2fCAS | 22335501PubMed |

Massonnet C, Vile D, Fabre J, Hannah MA, Caldana C, Lisec J, Beemster GT, Meyer RC, Messerli G, Gronlund JT, Perkovic J, Wigmore E, May S, Bevan MW, Meyer C, Rubio-Díaz S, Weigel D, Micol JL, Buchanan-Wollaston V, Fiorani F, Walsh S, Rinn B, Gruissem W, Hilson P, Hennig L, Willmitzer L, Granier C (2010) Probing the reproducibility of leaf growth and molecular phenotypes: a comparison of three Arabidopsis accessions cultivated in ten laboratories. Plant Physiology 152, 2142–2157.
Probing the reproducibility of leaf growth and molecular phenotypes: a comparison of three Arabidopsis accessions cultivated in ten laboratories.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmsVantrw%3D&md5=079e0c13722a4a8a4cde11928cd1b7d4CAS | 20200072PubMed |

Mathieu A, Cournède PH, Letort V, Barthélémy D, de Reffye P (2009) A dynamic model of plant growth with interactions between development and fucntional mechanisms to study plant structrual plasticity related to trophic competition. Annals of Botany 103, 1173–1186.
A dynamic model of plant growth with interactions between development and fucntional mechanisms to study plant structrual plasticity related to trophic competition.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MzntVWjtw%3D%3D&md5=919678c4156e750dcd101a5a110ce35eCAS | 19297366PubMed |

Muller B, Pantin F, Génard M, Turc O, Freixes S, Picques M, Gibon Y (2011) Water deficit uncouple growth form photosynthesis, increase C content and modify the relationships between C and growth in sink organs. Journal of Experimental Botany 62, 1715–1729.
Water deficit uncouple growth form photosynthesis, increase C content and modify the relationships between C and growth in sink organs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjsFyjtbc%3D&md5=99ab45722cfcc7537b4cf35b2d76a6daCAS | 21239376PubMed |

Pallas B, Louarn G, Christophe A, Lebon E, Lecoeur J (2008) Influence of intra-shoot trophic competition on shoot development in two grapevine cultivars. Physiologia Plantarum 134, 49–63.
Influence of intra-shoot trophic competition on shoot development in two grapevine cultivars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFChtb3F&md5=023e1c4e5e735d835ab82cffbd7e6f0dCAS | 18399930PubMed |

Pallas B, Christophe A, Cournède PH, Lecoeur J (2009) Using a mathematical model to evaluate the trophic and non-trophic determinants of axis development in grapevine. Functional Plant Biology 36, 156–170.
Using a mathematical model to evaluate the trophic and non-trophic determinants of axis development in grapevine.Crossref | GoogleScholarGoogle Scholar |

Pallas B, Christophe A, Lecoeur J (2010) Are the common assimilate pool and trophic relationships appropriate for dealing with the observed plasticity of grapevine development? Annals of Botany 105, 233–247.
Are the common assimilate pool and trophic relationships appropriate for dealing with the observed plasticity of grapevine development?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c%2FnsV2ltA%3D%3D&md5=6985a283468f2457919e7edc38423453CAS | 19946042PubMed |

Pallas B, Loi C, Christophe A, Cournède PH, Lecoeur J (2011) Comparison of three approaches to model grapevine organogenesis in conditions of fluctuating temperature, solar radiation and soil water content. Annals of Botany 107, 729–745.
Comparison of three approaches to model grapevine organogenesis in conditions of fluctuating temperature, solar radiation and soil water content.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MvjvVKgsg%3D%3D&md5=e2c232c2ac983863c8c7509d1b47d878CAS | 20852307PubMed |

Pallas B, Clément-Vidal A, Rebolledo MC, Soulié JC, Luquet D (2013) Using plant growth modeling to analyze C source–sink relations under drought: inter and intraspecific comparison. Frontiers in Plant Science 4, 437
Using plant growth modeling to analyze C source–sink relations under drought: inter and intraspecific comparison.Crossref | GoogleScholarGoogle Scholar | 24204372PubMed |

Pellegrino A, Lebon E, Simonneau T, Wery J (2005) Towards a simple indicator of water stress in grapevine (Vitis vinifera L.) based on the differential sensitivities of vegetative growth components. Australian Journal of Grape and Wine Research 11, 306–315.
Towards a simple indicator of water stress in grapevine (Vitis vinifera L.) based on the differential sensitivities of vegetative growth components.Crossref | GoogleScholarGoogle Scholar |

Poorter H, Nagel O (2000) The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review. Australian Journal of Plant Physiology 27, 595–607.
The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlslars7w%3D&md5=51bd4a479a8428daaa3c102c1637d65bCAS |

Prieto JA, Louarn G, Peña Perez J, Ojeda H, Simonneau T, Lebon E (2012) A leaf gas exchange model that accounts for intra-canopy variability by considering leaf nitrogen content and local acclimation to radiation in grapevine (Vitis vinifera L.). Plant, Cell & Environment 35, 1313–1328.
A leaf gas exchange model that accounts for intra-canopy variability by considering leaf nitrogen content and local acclimation to radiation in grapevine (Vitis vinifera L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Git77J&md5=6c5601869991e16e7cb83d7d018a7957CAS |

R Development Core Team 2007. ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna)

Rives M (2000) Vigour, pruning, cropping in the grapevine (Vitis vinifera L.). I. A literature review. Agronomie 20, 79–91.
Vigour, pruning, cropping in the grapevine (Vitis vinifera L.). I. A literature review.Crossref | GoogleScholarGoogle Scholar |

Robin C, Hay MJM, Newton PCD, Greer DH (1994) Effect of light quality (red : far red ratio) at the apical bud of the main stolon morphogenesis of Trifolium repens L. Annals of Botany 74, 119–123.
Effect of light quality (red : far red ratio) at the apical bud of the main stolon morphogenesis of Trifolium repens L.Crossref | GoogleScholarGoogle Scholar |

Sala A, Woodruff DR, Meinzer FC (2012) Carbon dynamics in trees: feast or famine? Tree Physiology 32, 764–775.
Carbon dynamics in trees: feast or famine?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFClu7fI&md5=60a3af3278d49ec761a2214a7dc48e21CAS | 22302370PubMed |

Schultz HR (1992) An empirical model for the simulation of leaf appearance rate and leaf development of primary shoots of several grapevine (Vitis vinifera L.) canopy-systems. Scientia Horticulturae 52, 179–200.
An empirical model for the simulation of leaf appearance rate and leaf development of primary shoots of several grapevine (Vitis vinifera L.) canopy-systems.Crossref | GoogleScholarGoogle Scholar |

Seleznyova AN, Greer DH (2001) Effects of temperature and leaf position on leaf area expansion of kiwifruit (Actinidia deliciosa) shoots: development of a modelling framework. Annals of Botany 88, 605–615.
Effects of temperature and leaf position on leaf area expansion of kiwifruit (Actinidia deliciosa) shoots: development of a modelling framework.Crossref | GoogleScholarGoogle Scholar |

Sinclair TR, Ludlow MM (1986) Influence of soil water supply on the plant water balance of four tropical grain legumes. Australian Journal of Plant Physiology 13, 329–341.
Influence of soil water supply on the plant water balance of four tropical grain legumes.Crossref | GoogleScholarGoogle Scholar |

Sinoquet H, Le Roux X, Adam B, Ameglio T, Daudet FA (2001) RATP: a model for simulating the spatial distribution of radiation absorption, transpiration and photosynthesis within canopies: application to an isolated tree crown. Plant, Cell & Environment 24, 395–406.
RATP: a model for simulating the spatial distribution of radiation absorption, transpiration and photosynthesis within canopies: application to an isolated tree crown.Crossref | GoogleScholarGoogle Scholar |

Sobeih WY, Dodd IC, Bacon MA, Grierson D, Davies WJ (2004) Long-distance signals regulating stomatal conductance and leaf growth in tomato (Lycopersicon esculentum) plants subjected to partial root-zone drying. Journal of Experimental Botany 55, 2353–2363.
Long-distance signals regulating stomatal conductance and leaf growth in tomato (Lycopersicon esculentum) plants subjected to partial root-zone drying.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVOju7c%3D&md5=2ace1f0fe489ca726651727184703c95CAS | 15310826PubMed |

Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends in Plant Science 5, 537–542.
Phenotypic plasticity for plant development, function and life history.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7gvVenuw%3D%3D&md5=f257c24cfa7d4b863ed8cef10b667320CAS | 11120476PubMed |

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. Coordinating processes without an orchestrator? Current Opinion in Plant Biology 14, 283–289.
Water deficit and growth. Coordinating processes without an orchestrator?Crossref | GoogleScholarGoogle Scholar | 21388861PubMed |

Turc O, Lecoeur J (1997) Leaf primordium initiation and expanded leaf production are co-ordinated response to air temperature in pea (Pisum sativum L.). Annals of Botany 80, 265–273.
Leaf primordium initiation and expanded leaf production are co-ordinated response to air temperature in pea (Pisum sativum L.).Crossref | GoogleScholarGoogle Scholar |

Vile D, Garnier E, Shipley B, Laurenti G, Navas ML, Roumet C, Lavorel S, Diaz S, Hodgson JG, Lloret F, Midgley G, Poorter H, Rutherford M, Wilson P, Wright IJ (2005) Specific leaf area and dry matter content estimate thickness in laminar leaves. Annals of Botany 96, 1129–1136.
Specific leaf area and dry matter content estimate thickness in laminar leaves.Crossref | GoogleScholarGoogle Scholar | 16159941PubMed |

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 |

Yan HP, Kang MZ, de Reffye P, Dingkuhn M (2004) A dynamic, architectural plant model simulating resource-dependent growth. Annals of Botany 93, 591–602.
A dynamic, architectural plant model simulating resource-dependent growth.Crossref | GoogleScholarGoogle Scholar | 15056562PubMed |