Theoretical and Applied Genetics

, Volume 131, Issue 4, pp 903–915 | Cite as

Genetic architecture of aerial and root traits in field-grown grafted grapevines is largely independent

  • Jean-Pascal Tandonnet
  • Elisa Marguerit
  • Sarah J. Cookson
  • Nathalie Ollat
Original Article


Key message

QTLs were identified for traits assessed on field-grown grafted grapevines. Root number and section had the largest phenotypic variance explained. Genetic control of root and aerial traits was independent.


Breeding new rootstocks for perennial crops remains challenging, mainly because of the number of desirable traits which have to be combined, these traits include good rooting ability and root development. Consequently, the present study analyzes the genetic architecture of root traits in grapevine. A segregating progeny of 138 F1 genotypes issued from an inter-specific cross between Vitis vinifera cv. Cabernet-Sauvignon × V. riparia cv. Gloire de Montpellier, used as rootstock, was phenotyped in grafted plants grown for 2 years in the field. Seven traits, related to aerial and root development, were quantified. Heritability ranged between 0.44 for aerial biomass to 0.7 for root number. Total root number was related to the number of fine roots, while root biomass was related to the number of coarse roots. Significant quantitative trait loci (QTLs) were identified for all the traits studied with some of them explaining approximately 20% of phenotypic variance. Only a single QTL co-localized for root and aerial biomass. Identified QTLs for aerial-to-root biomass ratio suggest that aerial and root traits are controlled independently. Genes known to be involved in auxin signaling pathways and phosphorus nutrition, whose orthologues were previously shown to regulate root development in Arabidopsis, were located in the confidence intervals of several QTLs. This study opens new perspectives for breeding rootstocks with improved root development capacities.



We would like to acknowledge the excellent assistance of Louis Bordenave, Bernard Douens, Cyril Hévin, Jean-Pierre Petit and Jean-Paul Robert for the plant material grafting. We are also grateful to Pr. Gregory A. Gambetta and Dr. Philippe Vivin for critical reading and improvement of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

Informed consent was obtained from all individual participants included in this study.

Supplementary material

122_2017_3046_MOESM1_ESM.pdf (546 kb)
Supplementary material 1 (PDF 545 kb)


  1. Bavaresco L, Fregoni M, Perino A (1994) Physiological aspects of lime-induced chlorosis in some Vitis species. I. Pot trial on calcareous soil. Vitis 33:123–126Google Scholar
  2. Bellini C, Pacurar DI, Perrone I (2014) Adventitious roots and lateral roots: similarities and differences. Annu Rev Plant Biol 65:639–666CrossRefPubMedGoogle Scholar
  3. Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602CrossRefPubMedGoogle Scholar
  4. Bert PF, Bordenave L, Donnart M, Hevin C, Dodane JP, Ollat N, Decroocq S (2013) Mapping genetic loci for tolerance to lime induced iron deficiency chlorosis in grapevine rootstocks (Vitis sp). Theor Appl Genet 126:451–473CrossRefPubMedGoogle Scholar
  5. Bouteillé M, Rolland G, Balsera C, Loudet O, Muller B (2012) Disentangling the intertwined genetic bases of root and shoot growth in Arabidopsis. PLoS ONE 7:1–13CrossRefGoogle Scholar
  6. Branas J, Vergne A (1957) Morphologie du système radiculaire. Prog Agric Vitic 74:29–32Google Scholar
  7. Brunner I, Herzog C, Dawes MA, Arend M, Sperisen C (2015) How tree roots respond to drought. Front Plant Sci 6:547CrossRefPubMedPubMedCentralGoogle Scholar
  8. Clingeleffer P, Smith BP (2011) Rootstock breeding and development for Australian wine grapes. In: Final report. Project number CSP 05/03. GWRDC, p 98Google Scholar
  9. Comas LH, Becker SR, Cruz VMV, Byme PF, Dierig DA (2013) Root traits contributing to plant productivity under drought. Front Plant Sci 4:1–16CrossRefGoogle Scholar
  10. Courtois B, Ahmadi N, Khowaja F, Price AH, Rami J-F, Frouin J, Hamelin C, Ruiz M (2009) Rice root genetic architecture: meta-analysis from a drought QTL database. Rice 2:115–128CrossRefGoogle Scholar
  11. De Smet I, Vassileva V, De Rybel B, Levesque MP, Grunewald W, Van Damme D, Van Noorden G, Naudts M, Van Isterdael G, De Clercq R, Wang JY, Meuli N, Vanneste S, Friml J, Hilson P, Jürgens G, Ingram GC, Inzé D, Benfey PN, Beeckman T (2008) Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science 322:594–597CrossRefPubMedGoogle Scholar
  12. Den Herder G, van Isterdael G, Beeckman T, De Smet I (2010) The roots of a new green revolution. Trends Plant Sci 15:600–607CrossRefGoogle Scholar
  13. Dievart A, Coudert Y, Gantet P, Pauluzzi G, Puig J, Fanchon D, Ahmadi N, Courtois B, Guiderdoni E, Périn C (2013) Dissection des bases biologiques de caractères d’intérêt chez le riz: architecture et développement du système racinaire. Cah Agric 22:475–483Google Scholar
  14. Druege U, Franken P, Hajirezaei MR (2016) Plant hormone homeostasis, signaling, and function during adventitious root formation in cuttings. Front Plant Sci. PubMedPubMedCentralGoogle Scholar
  15. Fort KP, Fraga J, Grossi D, Walker AM (2017) Early measures of drought tolerance in four grape rootstocks. J Am Soc Hortic Sci 142:36–46CrossRefGoogle Scholar
  16. Gallais A (1990) Théorie de la sélection en amélioration des plantes. Masson, ParisGoogle Scholar
  17. Grattapaglia D, Bertolucci FL, Sederoff RR (1995) Genetic mapping of QTLs controlling vegetative propagation in Eucalyptus grandis and E. urophylla using a pseudo-testcross strategy and RAPD markers. Theor Appl Genet 90:933–947CrossRefPubMedGoogle Scholar
  18. Gruber B, Kosegarten H (2002) Depressed growth of non-chlorotic vine grown in calcareous soil is an iron deficiency symptom prior to leaf chlorosis. J Plant Nutr Soil Sci 165:111–117CrossRefGoogle Scholar
  19. Humphrey TV, Haasen KE, Aldea-Brydges MG, Sun H, Zayed Y, Indriolo E, Goring DR (2015) PERK–KIPK–KCBP signalling negatively regulates root growth in Arabidopsis thaliana. J Exp Bot 66:71–83CrossRefPubMedGoogle Scholar
  20. Ivanchenko MG, Muday GK, Dubrovsky JG (2008) Ethylene–auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana. Plant J 55:335–347CrossRefPubMedGoogle Scholar
  21. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyère C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Le Clainche I, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave F, Pé ME, Valle G, Morgante M, Caboche M, Adam-Blondon AF, Weissenbach J, Quétier F, Wincker P (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467CrossRefPubMedGoogle Scholar
  22. Janiak A, Kwaśniewski M, Szarejko I (2016) Gene expression regulation in roots under drought. J Exp Bot 67:1003–1014CrossRefPubMedGoogle Scholar
  23. Karthikeyan AS, Varadarajan DK, Jain A, Held MA, Carpita NC, Raghothama KG (2007) Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta 225:907–918CrossRefPubMedGoogle Scholar
  24. Kroymann J, Mitchell-Olds T (2005) Epistasis and balanced polymorphism influencing complex trait variation. Nature 435:95–98CrossRefPubMedGoogle Scholar
  25. Lecourt J, Lauvergeat V, Ollat N, Vivin P, Cookson SJ (2015) Shoot and root ionome responses to nitrate supply in grafted grapevines are rootstock genotype dependent. Aust J Grape Wine Res. Google Scholar
  26. Legué V, Rigal A, Bhalerao RP (2014) Adventitious root formation in tree species: involvement of transcription factors. Physiol Plant 151:192–198CrossRefPubMedGoogle Scholar
  27. Liang Q, Li P, Hua H, Li Z, Rong Y, Wang K, Hua J (2014) Dynamic QTL and epistasis analysis on seedling root traits in upland cotton. J Genet 93:63–78CrossRefPubMedGoogle Scholar
  28. López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Pérez-Torres A, Rampey RA, Bartel B, Herrera-Estrella L (2005) An auxin transport independent pathway is involved in phosphate stress-induced root architectural alterations in Arabidopsis. Identification of BIG as a mediator of auxin in pericycle cell activation. Plant Physiol 137:681–691CrossRefPubMedPubMedCentralGoogle Scholar
  29. Maccaferri M, El-Feki W, Nazemi G, Salvi S, Canè MA, Colalongo MC, Stefanelli S, Tuberosa R (2016) Prioritizing quantitative trait loci for root system architecture in tetraploid wheat. J Exp Bot 67:1161–1178CrossRefPubMedPubMedCentralGoogle Scholar
  30. Mai CD, Phung NT, To HT, Gonin M, Hoang GT, Nguyen KL, Do VN, Courtois B, Gantet P (2014) Genes controlling root development in rice. Rice 7:30CrossRefPubMedPubMedCentralGoogle Scholar
  31. Marchant A, Bhalerao R, Casimiro I, Eklöf J, Casero PJ, Bennett M, Sandberg G (2002) AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. Plant Cell 14:589–597CrossRefPubMedPubMedCentralGoogle Scholar
  32. Marguerit E, Némorin A, Manicki A, Boury C, Donnart M, Butterlin G, Merdinoglu D, Ollat N, Decroocq S (2009) Genetic dissection of sex determinism, inflorescence morphology and downy mildew resistance in grapevine. Theor Appl Genet 118:1261–1278CrossRefPubMedGoogle Scholar
  33. 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 Phytol 194:416–429CrossRefPubMedGoogle Scholar
  34. Marhavý P, Vanstraelen M, De Rybel B, Zhaojun D, Bennett MJ, Beeckman T, Benková E (2013) Auxin reflux between the endodermis and pericycle promotes lateral root initiation. EMBO J 32:149–158CrossRefPubMedGoogle Scholar
  35. Marques CM, Vasquez-Kool J, Carocha VJ, Ferreira JG, O’Malley DM, Liu B-H, Sederoff R (1999) Genetic dissection of vegetative propagation traits in Eucalyptus tereticornis and E. globulus. Theor Appl Genet 99:936–946CrossRefGoogle Scholar
  36. McConnaughay KDM, Coleman JS (1999) Biomass allocation in plants: ontogeny or optimality? A test along three resource gradients. Ecology 80:2581–2593CrossRefGoogle Scholar
  37. Meister R, Rajani MS, Ruzicka D, Schachtman DP (2014) Challenges of modifying root traits in crops for agriculture. Trends Plants Sci 19:779–788CrossRefGoogle Scholar
  38. Miura K, Lee J, Gong Q, Ma S, Jin JB, Yoo CY, Miura T, Sato A, Bohnert HJ, Hasegawa PM (2011) SIZ1 regulation of phosphate starvation-induced root architecture remodeling involves the control of auxin accumulation. Plant Physiol 155:1000–1012CrossRefPubMedGoogle Scholar
  39. Moriya S, Iwanami H, Haji T, Okada K, Yamada M, Yamamoto T, Abe K (2015) Identification and genetic characterization of a quantitative trait locus for adventitious rooting from apple hardwood cuttings. Tree Genet Genome 59:1–11Google Scholar
  40. 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. Funct Plant Biol 39:891–904CrossRefGoogle Scholar
  41. Negi S, Sukumar P, Liu X, Cohen JD, Muday GK (2010) Genetic dissection of the role of ethylene in regulating auxin-dependent lateral and adventitious root formation in tomato. Plant J 61:3–15CrossRefPubMedGoogle Scholar
  42. Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguchi C (2004) Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16:1365–1377CrossRefPubMedPubMedCentralGoogle Scholar
  43. Niu YF, Chai RS, Jin GL, Wang H, Tang CX, Zhang YS (2013) Responses of root architecture development to low phosphorus availability: a review. Ann Bot 112:391–408CrossRefPubMedGoogle Scholar
  44. Paez-Garcia A, Motes CM, Scheible WR, Chen R, Blancaflor EB, Monteros MJ (2015) Root traits and phenotyping strategies for plant improvement. Plants 4:334–355CrossRefPubMedPubMedCentralGoogle Scholar
  45. Parelle J, Zapater M, Scotti-Saintagne C, Kremer A, Jolivet Y, Dreyer E, Brendel O (2007) Quantitative trait loci of tolerance to waterlogging in a European oak (Quercus robur L.): physiological relevance and temporal effect patterns. Plant Cell Environ 30:422–434CrossRefPubMedGoogle Scholar
  46. Passioura JB (2006) The perils of pot experiments. Funct Plant Biol 33:1075–1079CrossRefGoogle Scholar
  47. Perry RL, Lyda SD, Bowen HH (1983) Root distribution of four Vitis cultivars. Plant Soil 71:63–74CrossRefGoogle Scholar
  48. Pongracz DP (1983) Rootstocks for grape-vines. David Philip, Cape TownGoogle Scholar
  49. Poorter H, Jagodzinski AM, Ruiz-Peinado R, Kuyah S, Luo Y, Oleksyn J, Usoltsev VA, Buckley TN, Reich PB, Sack L (2015) How does biomass distribution change with size and differ among species? An analysis for 1200 plant species from five continents. New Phytol 208:736–749CrossRefPubMedPubMedCentralGoogle Scholar
  50. Price AH (2006) Believe it or not, QTLs are accurate! Trends Plant Sci 11:213–216CrossRefPubMedGoogle Scholar
  51. Prinzenberg AE, Barbier H, Salt DE, Stich B, Reymond M (2010) Relationships between growth, growth response to nutrient supply, and ion content using a recombinant inbred line population in Arabidopsis. Plant Physiol 154:1361–1371CrossRefPubMedPubMedCentralGoogle Scholar
  52. Ramírez-Carvajal GA, Morse AM, Dervinis C, Davis JM (2009) The cytokinin type-B response regulator PtRR13 is a negative regulator of adventitious root development in Populus. Plant Physiol 150:759–771CrossRefPubMedPubMedCentralGoogle Scholar
  53. Rebaï A (1997) Comparison of methods for regression interval mapping in QTL analysis with non-normal traits. Genet Res 69:69–74CrossRefGoogle Scholar
  54. Ribeiro CL, Silva CM, Drost DR, Novaes E, Novaes CRDB, Dervinis C, Kirst M (2016) Integration of genetic, genomic and transcriptomic information identifies putative regulators of adventitious root formation in Populus. BMC Plant Biol 16:66CrossRefPubMedPubMedCentralGoogle Scholar
  55. Rogg LE, Lasswell J, Bartel B (2001) A gain-of-function mutation in IAA28 suppresses lateral root development. Plant Cell 13:465–480CrossRefPubMedPubMedCentralGoogle Scholar
  56. Rönnberg-Wästljung AC, Glynn C, Weih M (2005) QTL analyses of drought tolerance and growth for a Salix dasyclados × Salix viminalis hybrid in contrasting water regimes. Theor Appl Genet 110:537–549CrossRefPubMedGoogle Scholar
  57. Scotti-Saintagne C, Bertocchi E, Barreneche T, Kremer A, Plomion C (2005) Quantitative trait loci mapping for vegetative propagation in pedunculate oak. Ann For Sci 62:369–374CrossRefGoogle Scholar
  58. Shepherd M, Mellick R, Toon P, Dale G, Dieters M (2005) Genetic control of adventitious rooting on stem cuttings in two Pinus elliottii × P. caribaea hybrid families. Ann Sci For 62:403–412CrossRefGoogle Scholar
  59. Shepherd M, Huang S, Eggler P, Cross M, Dale G, Dieters M, Henry R (2006) Congruence in QTL for adventitious rooting in Pinus elliottii × Pinus caribaea hybrids resolves between and within-species effects. Mol Breed 18:11–28CrossRefGoogle Scholar
  60. Shepherd M, Kasem S, Lee DJ, Henry R (2008) Mapping species differences for adventitious rooting in a Corymbia torelliana × Corymbia citriodora subspecies variegata hybrid. Tree Genet Genomes 4:715–725CrossRefGoogle Scholar
  61. Slovak R, Ogura T, Satbhai SB, Ristova D, Busch W (2016) Genetic control of root growth: from genes to networks. Ann Bot 117:9–24CrossRefPubMedGoogle Scholar
  62. Smart DR, Schwass E, Lakso A, Morano L (2006) Grapevine rooting patterns: a comprehensive analysis and a review. Am J Enol Vitic 57:89–104Google Scholar
  63. Smith BP (2010) Genetic and molecular mapping studies on a population derived from Vitis vinifera × Muscadinia rotundifolia and genetic diversity of wild Muscadinia rotundifolia. University of California, Davis, p 268Google Scholar
  64. Smith BP, Matthew SW, Jones TH, Morales NB, Clingeleffer PR (2013) Heritability of adventitious rooting of grapevine dormant canes. Tree Genet Genomes 9:467–474CrossRefGoogle Scholar
  65. Southey JM, Archer E (1988) The effect of rootstock cultivar on grapevine root distribution and density. In: Van Zyl JL (ed) The grapevine root and its environment. Department of Agriculture and Water Supply, Pretoria, pp 57–73Google Scholar
  66. Swanepoel JJ, Southey JM (1989) The influence of rootstock on the rooting pattern of the grapevine. S Afr J Enol Vitic 10:23–28Google Scholar
  67. Tandonnet JP, Cookson SJ, Vivin P, Ollat N (2010) Scion control biomass allocation and root development in grafted grapevines. Aust J Grape Wine Res 16:290–300CrossRefGoogle Scholar
  68. Uga Y, Okuno K, Yano M (2011) Dro1, a major QTL involved in deep rooting of rice under upland field conditions. J Exp Bot 62:2485–2494CrossRefPubMedGoogle Scholar
  69. Van Ooijen JW (2009) MapQTL 6. Software for the mapping of quantitative trait loci in experimental populations of diploid species. B.V. Kyazma, WageningenGoogle Scholar
  70. Wu Q, Pagès L, Wu J (2016) Relationships between root diameter, root length and root branching along lateral roots in adult, field-grown maize. Ann Bot 117:379–390CrossRefPubMedPubMedCentralGoogle Scholar
  71. Wullschleger SD, Yin TM, DiFazio SP, Tschaplinski TJ, Gunter LE, Davis MF, Tuskan GA (2005) Phenotypic variation in growth and biomass distribution for two advances-generation pedigrees of hybrid poplar. Can J For Res 35:1779–1789CrossRefGoogle Scholar
  72. Zhang B, Tong C, Yin T, Zhang X, Zhuge Q, Huang M, Wang M, Wu R (2009) Detection of quantitative trait loci influencing growth trajectories of adventitious roots in Populus using functional mapping. Tree Genet Genomes 5:539–552CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.EGFV, Bordeaux Sciences Agro, INRAUniversity of BordeauxVillenave d’OrnonFrance

Personalised recommendations