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Identifying Developmental Patterns in Structured Plant Phenotyping Data

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Plant Systems Biology

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2395))

Abstract

Technological breakthroughs concerning both sensors and robotized plant phenotyping platforms have totally renewed the plant phenotyping paradigm in the last two decades. This has impacted both the nature and the throughput of data with the availability of data at high-throughput from the tissular to the whole plant scale. Sensor outputs often take the form of 2D or 3D images or time series of such images from which traits are extracted while organ shapes, shoot or root system architectures can be deduced. Despite this change of paradigm, many phenotyping studies often ignore the structure of the plant and therefore loose the information conveyed by the temporal and spatial patterns emerging from this structure. The developmental patterns of plants often take the form of succession of well-differentiated phases, stages or zones depending on the temporal, spatial or topological indexing of data. This entails the use of hierarchical statistical models for their identification.

The objective here is to show potential approaches for analyzing structured plant phenotyping data using state-of-the-art methods combining probabilistic modeling, statistical inference and pattern recognition. This approach is illustrated using five different examples at various scales that combine temporal and topological index parameters, and development and growth variables obtained using prospective or retrospective measurements.

Yann Guédon was passed away.

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References

  1. Tardieu F, Cabrera-Bosquet L, Pridmore T et al (2017) Plant phenomics, from sensors to knowledge. Curr Biol 27:770–783

    Article  Google Scholar 

  2. Tisné S, Reymond M, Vile D et al (2008) Combined genetic and modeling approaches reveal that epidermal cell area and number in leaves are controlled by leaf and plant developmental processes in Arabidopsis. Plant Physiol 148:1117–1127

    Article  PubMed  PubMed Central  Google Scholar 

  3. Bac-Molenaar JA, Vreugdenhil D, Granier C et al (2015) Genome wide association mapping of growth dynamics detects time-specific and general QTLs. J Exp Bot 66:5567–5580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Alvarez PS, Cabrera-Bosquet L, Grau A et al (2018) Phenomics allows identification of genomic regions affecting maize stomatal conductance with conditional effects of water deficit and evaporative demand. Plant Cell Environ 41:314–326

    Article  Google Scholar 

  5. Galvan-Ampudia CS, Chaumeret AM, Godin C et al (2016) Phyllotaxis: from patterns of organogenesis at the meristem to shoot architecture. Wiley Interdiscip Rev Dev Biol 5:460–473

    Article  PubMed  Google Scholar 

  6. Hallé F, Oldeman R (1970) Essai sur l'architecture et la dynamique de croissance des arbres tropicaux. Masson, Paris

    Google Scholar 

  7. Oldeman RAA (1983) Tropical rain forest, architecture, silvigenesis and diversity. In: Sutton SL, Whitmore TC, Chadwick AC (eds) Tropical rain forest: ecology and management. Blackwell, Oxford, pp 139–150

    Google Scholar 

  8. Barthélémy D, Edelin C, Hallé F (1991) Canopy architecture. In: Raghavendra AS (ed) Physiology of trees. John Wiley and Sons, Ltd, Chichester, pp 1–20

    Google Scholar 

  9. Barthélémy D, Caraglio Y (2007) Plant architecture: a dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny. Ann Bot 99:375–407

    Article  PubMed  PubMed Central  Google Scholar 

  10. Wilcox HE (1969) Morphologieal studies of the root system of red pine, Pinus resinosa Ait, I: growth characteristics and pattern of branching. Am J Bot 55:247–254

    Article  Google Scholar 

  11. Wigthman F, Thimann KV (1980) Hormonal factors controlling the initiation and development of lateral roots 1: sources of primordia inducing substances in the primary root of pea seedlings. Physiol Plant 49:13–20

    Article  Google Scholar 

  12. Nozeran R, Bancilhon L, Neuville P (1971) Intervention of internal correlations in morphogenesis of higher plants. Adv Morphog 9:1–66

    Article  CAS  PubMed  Google Scholar 

  13. Champagnat P (1989) Rest and activity in vegetative buds of trees. Ann Sci For 46:9–26

    Article  Google Scholar 

  14. Du Y, Scheres B (2017) Lateral root formation and the multiple roles of auxin. J Exp Bot 69:155–167

    Article  Google Scholar 

  15. Waters MT, Gutjahr C, Bennett T et al (2017) Strigolactone signaling and evolution. Annu Rev Plant Biol 68:291–322

    Article  CAS  PubMed  Google Scholar 

  16. Domagalska MA, Leyser O (2011) Signal integration in the control of shoot branching. Nat Rev Mol Cell Biol 12:211

    Article  CAS  PubMed  Google Scholar 

  17. Chomicki G, Coiro M, Renner SS (2017) Evolution and ecology of plant architecture: integrating insights from the fossil record, extant morphology, developmental genetics and phylogenies. Ann Bot 120:855–891

    Article  PubMed  PubMed Central  Google Scholar 

  18. Lehnebach R, Beyer R, Letort V et al (2018) The pipe model theory half a century on: a review. Ann Bot 121:773–795

    Article  PubMed  PubMed Central  Google Scholar 

  19. Lauri P-É (2019) Corner’s rules as a framework for plant morphology, architecture and functioning—issues and steps forward. New Phytol 221:1679–1684

    Article  PubMed  Google Scholar 

  20. Dang-Le AT, Edelin C, Le-Cong K (2013) Ontogenetic variations in leaf morphology of the tropical rain forest species Dipterocarpus alatus Roxb. Ex G Don Trees 27:773–786

    Google Scholar 

  21. Roggy JC, Nicolini E, Imbert P et al (2005) Links between tree structure and functional leaf traits in the tropical forest tree Dicorynia guianensis Amshoff (Caesalpiniaceae). Ann For Sci 62:553–564

    Google Scholar 

  22. Lucas M, Guédon Y, Jay-Allemand C et al (2008) An auxin transport-based model of root branching in Arabidopsis thaliana. PLoS One 3:e3673

    Article  PubMed  PubMed Central  Google Scholar 

  23. Heuret P, Guédon Y, Guérard N et al (2003) Analysing branching pattern in plantations of young red oak trees (Quercus rubra L., Fagaceae). Ann Bot 91:479–492

    Article  PubMed  PubMed Central  Google Scholar 

  24. Peyhardi J, Caraglio Y, Costes E et al (2017) Integrative models for joint analysis of shoot growth and branching patterns. New Phytol 216:1291–1304

    Article  CAS  PubMed  Google Scholar 

  25. Dutra SJ, Guédon Y, Herter FG et al (2014) Exploring bud dormancy completion with a combined architectural and phenological analysis: the case of the apple tree in contrasting winter temperature conditions. Am J Bot 101:398–407

    Article  Google Scholar 

  26. Kawamura K (2010) A conceptual framework for the study of modular responses to local environmental heterogeneity within the plant crown and a review of related concepts. Ecol Res 25:733–744

    Article  Google Scholar 

  27. Reddy GV, Gordon SP, Meyerowitz EM (2007) Unravelling developmental dynamics: transient intervention and live imaging in plants. Nat Rev Mol Cell Biol 8:491–501

    Article  CAS  PubMed  Google Scholar 

  28. Klemm M, Röttger O, Damerow L et al (2016) Non-invasive examination of plant surfaces by opto-electronic means − using russet as a prime example. Sensors 16:452

    Article  PubMed  PubMed Central  Google Scholar 

  29. Reynaud EG, Peychl J, Huisken J et al (2015) Guide to light-sheet microscopy for adventurous biologists. Nat Methods 12:30–34

    Article  CAS  PubMed  Google Scholar 

  30. Mooney S, Pridmore T, Helliwell J et al (2012) Developing X-ray computed tomography to non-invasively image 3-D root systems architecture in soil. Plant Soil 352:1–22

    Article  CAS  Google Scholar 

  31. Lafond JA, Han L, Dutilleul P (2015) Concepts and analyses in the CT scanning of root systems and leaf canopies: a timely summary. Front Plant Sci 6:1111

    Article  PubMed  PubMed Central  Google Scholar 

  32. Danjon F, Barker DH, Drexhage M et al (2007) Using three-dimensional plant root architecture in models of shallow-slope stability. Ann Bot 101:1281–1293

    Article  PubMed  PubMed Central  Google Scholar 

  33. Sinoquet H, Rivet P (1997) Measurement and visualization of the architecture of an adult tree based on a three-dimensional digitising device. Trees 11:265–270

    Article  Google Scholar 

  34. Dassot M, Constant T, Fournier M (2011) The use of terrestrial LiDAR technology in forest science: application fields, benefits and challenges. Ann For Sci 68:959–974

    Article  Google Scholar 

  35. Saarinen N, Kankare V, Vastaranta M et al (2017) Feasibility of terrestrial laser scanning for collecting stem volume information from single trees. ISPRS J Photogramm Remote Sens 123:140–158

    Article  Google Scholar 

  36. Liang X, Litkey P, Hyyppa J et al (2012) Automatic stem mapping using single-scan terrestrial laser scanning. IEEE Trans Geosci Remote Sens 50:661–670

    Article  Google Scholar 

  37. Bournez E, Landes T, Saudreau M et al (2017) From TLS point clouds to 3D models of trees: a comparison of existing algorithms for 3D tree reconstruction. Int Arch Photogramm Remote Sens Spat Inf Sci 42:113

    Article  Google Scholar 

  38. Hruska J, Čermák J, Šustek S (1999) Mapping tree root systems with ground-penetrating radar. Tree Physiol 19:125–130

    Article  PubMed  Google Scholar 

  39. Barton CV, Montagu KD (2004) Detection of tree roots and determination of root diameters by ground penetrating radar under optimal conditions. Tree Physiol 24:1323–1331

    Article  PubMed  Google Scholar 

  40. Van Do T, Osawa A, Sato T (2015) Estimation of fine-root production using rates of diameter-dependent root mortality, decomposition and thickening in forests. Tree Physiol 36:513–523

    PubMed  Google Scholar 

  41. Borden KA, Thomas SC, Isaac ME (2017) Interspecific variation of tree root architecture in a temperate agroforestry system characterized using ground-penetrating radar. Plant Soil 410:323–334

    Article  CAS  Google Scholar 

  42. Liu X, Cui X, Guo L et al (2019) Non-invasive estimation of root zone soil moisture from coarse root reflections in ground-penetrating radar images. Plant Soil 436:623–639

    Article  CAS  Google Scholar 

  43. Fahlgren N, Gehan MA, Baxter I (2015) Lights, camera, action: high-throughput plant phenotyping is ready for a close-up. Curr Opin Plant Biol 24:93–99

    Article  PubMed  Google Scholar 

  44. Pound MP, Atkinson JA, Townsend AJ et al (2017) Deep machine learning provides state-of-the-art performance in image-based plant phenotyping. GigaScience 6:1–10

    Article  PubMed  PubMed Central  Google Scholar 

  45. Goodfellow I, Bengio Y, Courville A (2016) Deep learning. The MIT Press, Cambridge

    Google Scholar 

  46. Dhondt S, Wuyts N, Inzé D (2013) Cell to whole-plant phenotyping: the best is yet to come. Trends Plant Sci 18:1360–1385

    Article  Google Scholar 

  47. Houle D, Govindaraju DR, Omholt S (2010) Phenomics: the next challenge. Nat Rev Genet 11:855–866

    Article  CAS  PubMed  Google Scholar 

  48. Diggle PJ, Heagerty P, Liang K-Y et al (2002) Analysis of longitudinal data, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  49. Cressie N, Wikle CK (2011) Statistics for Spatio-temporal data. Wiley, Hoboken

    Google Scholar 

  50. Fisher RA (1918) The correlation between relatives on the supposition of Mendelian inheritance. Trans Royal Soc Edinburgh 52:399–433

    Article  Google Scholar 

  51. de Villemereuil P (2018) Quantitative genetic methods depending on the nature of the phenotypic trait. Ann N Y Acad Sci 1422:29–47

    Article  PubMed  Google Scholar 

  52. Wasson AP, Chiu GS, Zwart AB et al (2017) Differentiating wheat genotypes by Bayesian hierarchical nonlinear mixed modeling of wheat root density. Front Plant Sci 8:282

    Article  PubMed  PubMed Central  Google Scholar 

  53. Schaller GE, Bishopp A, Kieber JJ (2015) The yin-yang of hormones: cytokinin and auxin interactions in plant development. Plant Cell 27:44–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Puig J, Pauluzzi G, Guiderdoni E et al (2012) Regulation of shoot and root development through mutual signaling. Mol Plant 5:974–983

    Article  CAS  PubMed  Google Scholar 

  55. Bishop CM (2006) Pattern recognition and machine learning. Springer, New York

    Google Scholar 

  56. Murphy KP (2012) Machine learning: a probabilistic perspective. The MIT press, Cambridge

    Google Scholar 

  57. Grenander U, Miller MI (2006) Pattern theory, from representation to inference. Oxford University Press, Oxford

    Book  Google Scholar 

  58. Hastie T, Tibshirani R, Friedman J (2009) The elements of statistical learning: data mining, inference and prediction, 2nd edn. Springer, New York

    Book  Google Scholar 

  59. MacKay DJC (2003) Information theory, inference and learning algorithms. Cambridge University Press, New York

    Google Scholar 

  60. Koller D, Friedman N (2009) Probabilistic graphical models: principles and techniques. The MIT Press, Cambridge

    Google Scholar 

  61. Guédon Y, Refahi Y, Besnard F et al (2013) Pattern identification and characterization reveal permutations of organs as a key genetically controlled property of post-meristematic phyllotaxis. J Theor Biol 338:94–110

    Article  PubMed  Google Scholar 

  62. Besnard F, Refahi Y, Morin V et al (2014) Cytokinin signalling inhibitory fields provide robustness to phyllotaxis. Nature 505:417–421

    Article  CAS  PubMed  Google Scholar 

  63. Costes E, Guédon Y (2012) Deciphering the ontogeny of a sympodial tree. Trees 26:865–879

    Article  Google Scholar 

  64. Durand J-B, Guitton B, Peyhardi J et al (2013) New insights for estimating the genetic value of segregating apple progenies for irregular bearing during first years of tree production. J Exp Bot 64:5099–5113

    Article  CAS  PubMed  Google Scholar 

  65. Durand J-B, Allard A, Guitton B et al (2017) Predicting flowering behavior and exploring its genetic determinism in an apple multi-family population based on statistical indices and simplified phenotyping. Front Plant Sci 8:858

    Article  PubMed  PubMed Central  Google Scholar 

  66. Moreno-Ortega B, Fort G, Muller B et al (2017) Identifying developmental zones in maize lateral root cell length profiles using multiple change-point models. Front Plant Sci 8:1750

    Article  PubMed  PubMed Central  Google Scholar 

  67. Passot S, Moreno-Ortega B, Moukouanga D et al (2018) A new phenotyping pipeline reveals three types of lateral roots and a random branching pattern in two cereals. Plant Physiol 177:896–910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Lièvre M, Granier C, Guédon Y (2016) Identifying developmental phases in Arabidospis thaliana rosette using integrative segmentation models. New Phytol 210:1466–1478

    Article  PubMed  Google Scholar 

  69. Cookson SJ, Chenu K, Granier C (2007) Day length affects the dynamics of leaf expansion and cellular development in Arabidopsis thaliana partially through floral transition timing. Ann Bot 99:703–711

    Article  PubMed  PubMed Central  Google Scholar 

  70. Tisné S, Barbier F, Granier C (2011) The ERECTA gene controls spatial and temporal patterns of epidermal cell number and size in successive developing leaves of Arabidopsis thaliana. Ann Bot 108:159–168

    Article  PubMed  PubMed Central  Google Scholar 

  71. Guédon Y, Barthélémy D, Caraglio Y et al (2001) Pattern analysis in branching and axillary flowering sequences. J Theor Biol 212:481–520

    Article  PubMed  Google Scholar 

  72. Dambreville A, Lauri P-É, Normand F et al (2015) Analysing growth and development of plants jointly using developmental growth stages. Ann Bot 115:93–105

    Article  PubMed  Google Scholar 

  73. Prats-Llinàs MT, Lopez G, Fyhrie K et al (2019) Long proleptic and sylleptic shoots in peach (Prunus persica L. Batsch) trees have similar, predetermined, maximum numbers of nodes and bud fate patterns. Ann Bot 123:993–1004

    Google Scholar 

  74. Perrotte J, Guédon Y, Gaston A et al (2016) Identification of successive flowering phases highlights a new genetic control of the flowering pattern in strawberry. J Exp Bot 67:5643–5655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Guédon Y, Costes E, Rakocevic M (2018) Identification of growth and resting phases in yerba-mate cultivated in agroforestry or monoculture during a two-year period. Ecol Model 384:188–197

    Article  Google Scholar 

  76. Guédon Y, Caraglio Y, Heuret P et al (2007) Analyzing growth components in trees. J Theor Biol 248:418–447

    Article  PubMed  Google Scholar 

  77. Chaubert-Pereira F, Caraglio Y, Lavergne C et al (2009) Identifying ontogenetic, environmental and individual components of forest tree growth. Ann Bot 104:883–896

    Article  PubMed  PubMed Central  Google Scholar 

  78. Taugourdeau O, Chaubert-Pereira F, Sabatier S et al (2011) Deciphering the developmental plasticity of walnut saplings in relation to climatic factors and light environment. J Exp Bot 62:5283–5296

    Article  CAS  PubMed  Google Scholar 

  79. Taugourdeau O, Caraglio Y, Sabatier S et al (2015) Characterizing the respective importance of ontogeny and environmental constraints in forest tree development using growth phase duration distributions. Ecol Model 300:61–72

    Article  Google Scholar 

  80. Taugourdeau O, Dauzat J, Griffon S et al (2012) Retrospective analysis of tree architecture in silver fir (Abies alba mill.): ontogenetic trends and responses to environmental variability. Ann For Sci 69:713–721

    Google Scholar 

  81. Lièvre M (2014) Multi-scale analysis and modeling of shoot growth in Arabidopsis thaliana, PhD thesis, Montpellier SupAgro

    Google Scholar 

  82. Hallé F, Oldeman RA, Tomlinson PB (1978) Tropical trees and forests: an architectural analysis. Springer, Berlin, Heidelberg

    Book  Google Scholar 

  83. Meicenheimer RD (1982) Change in Epilobium phyllotaxy during reproductive transition. Am J Bot 69:1108–1118

    Article  Google Scholar 

  84. Caraglio Y, Edelin C (1990) Architecture et dynamique de croissance du platane. Platanus hybrida Brot. (Platanaceae){Syn. Platanus acerifolia (Aiton) Willd.}. Bull. Soc. Bot. France 137:279–291

    Google Scholar 

  85. White J (1979) The plant as a metapopulation. Annu Rev Ecol Syst 10:109–145

    Article  Google Scholar 

  86. Critchfield WB (1971) Shoot growth and heterophylly in Acer. J Arnold Arboretum 52:240–266

    Google Scholar 

  87. Kukk M, Sõber A (2015) Bud development and shoot morphology in relation to crown location. AoB Plants 7:plv082

    Article  PubMed  PubMed Central  Google Scholar 

  88. Guédon Y, Puntieri JG, Sabatier S et al (2006) Relative extents of preformation and neoformation in tree shoots: analysis by a deconvolution method. Ann Bot 98:835–844

    Article  PubMed  PubMed Central  Google Scholar 

  89. Louarn G, Guédon Y, Lecoeur J et al (2007) Quantitative analysis of the phenotypic variability of shoot architecture in two grapevine cultivars (Vitis vinifera L.). Ann Bot 99:425–437

    Article  PubMed  PubMed Central  Google Scholar 

  90. Heuret P, Barthélémy D, Guédon Y et al (2002) Synchronization of growth, branching, and flowering processes in the south American tropical tree Cecropia obtusa (Cecropiaceae). Am J Bot 89:1180–1187

    Google Scholar 

  91. Zalamea PC, Stevenson PR, Madriñán S et al (2008) Growth pattern and age determination for Cecropia sciadophylla (Urticaceae). Am J Bot 95:263–271

    Google Scholar 

  92. Morel H, Mangenet T, Beauchêne J et al (2015) Seasonal variations in phenological traits: leaf shedding and cambial activity in Parkia nitida Miq. and Parkia velutina Benoist (Fabaceae) in tropical rainforest. Trees 29:973–984

    Google Scholar 

  93. Costes E, Guédon Y (1997) Modeling the sylleptic branching on one-year-old trunks of apple cultivars. J Am Soc Hortic Sci 122:53–62

    Article  Google Scholar 

  94. Costes E, Guédon Y (2002) Modelling branching patterns on 1-year-old trunks of six apple cultivars. Ann Bot 89:513–524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Renton M, Guédon Y, Godin C et al (2006) Similarities and gradients in growth-unit branching patterns during ontogeny in ‘Fuji’ apple trees: a stochastic approach. J Exp Bot 57:3131–3143

    Article  CAS  PubMed  Google Scholar 

  96. Negrón C, Contador ML, Lampinen BD et al (2013) Branching patterns and production of three almond cultivars with different tree architecture. J Am Soc Hortic Sci 138:407–415

    Article  Google Scholar 

  97. Negrón C, Contador ML, Lampinen BD et al (2014) Differences in shoot structure due to bud type, water deficit, and growth rate in almond trees (Prunus dulcis Mill.). Ann Bot 113:545–554

    Google Scholar 

  98. Negrón C, Contador ML, Lampinen BD et al (2015) How different pruning severities alters shoot structures: a modelling approach in young ‘nonpareil’ almond trees. Funct Plant Biol 42:325–335

    Article  PubMed  Google Scholar 

  99. Courbet F, Sabatier S, Guédon Y (2007) Predicting the vertical location of branches along atlas cedar stem (Cedrus atlantica Manetti) in relation to annual shoot length. Ann For Sci 64:707–718

    Google Scholar 

  100. Guédon Y, Heuret P, Costes E (2003) Comparison methods for branching and axillary flowering sequences. J Theor Biol 225:301–325

    Article  PubMed  Google Scholar 

  101. Han HH, Coutand C, Cochard H et al (2007) Effects of shoot bending on lateral fate and hydraulics – invariant and changing traits across five apple genotypes. J Exp Bot 58:3537–3547

    Article  CAS  PubMed  Google Scholar 

  102. Chabikwa TG, Brewer PB, Beveridge CA (2019) Initial bud outgrowth occurs independent of auxin flow out of buds. Plant Physiol 179:55–65

    Article  CAS  PubMed  Google Scholar 

  103. Durand J-B, Guédon Y, Caraglio Y et al (2005) Analysis of the plant architecture via tree-structured statistical models: the hidden Markov tree models. New Phytol 166:813–825

    Article  PubMed  Google Scholar 

  104. Muller B, Guédon Y, Lobet G et al (2019) Lateral roots: diversity in adversity. Trends Plant Sci 24:810–825

    Article  CAS  PubMed  Google Scholar 

  105. Nagel KA, Putz A, Gilmer F et al (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 39:891–904

    Article  PubMed  Google Scholar 

  106. Kim D-H, Kim J-H, Park J-H et al (2016) Correlation between above-ground and below-ground biomass of 13-year-old Pinus densiflora S. et Z. planted in a post-fire area in Samcheok. For Sci Technol 12:115–124

    Google Scholar 

  107. Rajashekar G, Fararoda R, Reddy RS et al (2018) Spatial distribution of forest biomass carbon (above and below ground) in Indian forests. Ecol Indic 85:742–752

    Article  CAS  Google Scholar 

  108. Zimmerman RH, Miller SS (1991) Orchard growth and fruiting of micropropagated apple trees. J Am Soc Hortic Sci 116:780–785

    Article  Google Scholar 

  109. Sinacore K, Hall JS, Potvin C et al (2017) Unearthing the hidden world of roots: root biomass and architecture differ among species within the same guild. PLoS One 12:e0185934

    Article  PubMed  PubMed Central  Google Scholar 

  110. Cermák J, Riguzzi F, Ceulemans R (1998) Scaling up from the individual tree to the stand level in scots pine. I. Needle distribution, overall crown and root geometry. Ann Sci For 55:63–88

    Article  Google Scholar 

  111. Lauri P-É, Maguylo K, Trottier C (2006) Architecture and size relations – an essay on apple (malus X domestica Borkh.) tree. Am J Bot 93:357–368

    Article  PubMed  Google Scholar 

  112. Willaume M, Pagès M (2006) How periodic growth pattern and source/sink relations affect root growth in oak tree seedlings. J Exp Bot 57:815–826

    Article  CAS  PubMed  Google Scholar 

  113. Bouteillé M, Rolland G, Balsera C et al (2012) Disentangling the intertwined genetic basis of root and shoot growth in Arabidopsis. PLoS One 7:e32319

    Article  PubMed  PubMed Central  Google Scholar 

  114. Fernique P, Dambreville A, Durand J-B. et al. (2016) Characterization of mango tree patchiness using a tree segmentation/clustering approach. In: proceedings of the IEEE international conference on functional-structural plant growth modeling, simulation, visualization and applications (FSPMA) pp. 68–74

    Google Scholar 

  115. Lobet G, Pound MP, Diener J et al (2015) Root system markup language: toward a unified root architecture description language. Plant Physiol 167:617–627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Godin C, Caraglio Y (1998) A multiscale model of plant topological structures. J Theor Biol 191:1–46

    Article  CAS  PubMed  Google Scholar 

  117. Dryden IL, Mardia KV (2016) Statistical shape analysis, with applications in R, 2nd edn. Wiley, Hoboken

    Book  Google Scholar 

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Guédon, Y., Caraglio, Y., Granier, C., Lauri, PÉ., Muller, B. (2022). Identifying Developmental Patterns in Structured Plant Phenotyping Data. In: Lucas, M. (eds) Plant Systems Biology. Methods in Molecular Biology, vol 2395. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-1816-5_10

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  • DOI: https://doi.org/10.1007/978-1-0716-1816-5_10

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