Genetic Analysis of Platform-Phenotyped Root System Architecture of Bread and Durum Wheat in Relation to Agronomic Traits

Roots are essential for water and nutrient uptake but are rarely the direct target of breeding efforts. To characterize the genetic variability of wheat root architecture, the root and shoot traits of 200 durum and 715 bread wheat varieties were measured at a young stage on a high-throughput phenotyping platform. Heritability of platform traits ranged from 0.40 for root biomass in durum wheat to 0.82 for the number of tillers. Field phenotyping data for yield components and SNP genotyping were already available for all the genotypes. Taking differences in earliness into account, several significant correlations between root traits and field agronomic performances were found, suggesting that plants investing more resources in roots in some stressed environments favored water and nutrient uptake, with improved wheat yield. We identified 100 quantitative trait locus (QTLs) of root traits in the bread wheat panels and 34 in the durum wheat panel. Most colocalized with QTLs of traits measured in field conditions, including yield components and earliness for bread wheat, but only in a few environments. Stress and climatic indicators explained the differential effect of some platform QTLs on yield, which was positive, null, or negative depending on the environmental conditions. Modern breeding has led to deeper rooting but fewer seminal roots in bread wheat. The number of tillers has been increased in bread wheat, but decreased in durum wheat, and while the root-shoot ratio for bread wheat has remained stable, for durum wheat it has been increased. Breeding for root traits or designing ideotypes might help to maintain current yield while adapting to specific drought scenarios.

[1]  M. F. Addis,et al.  Milk proteins as mastitis markers in dairy ruminants - a systematic review , 2022, Veterinary Research Communications.

[2]  Y. Trifa,et al.  Changes in yield and yield stability of durum wheat genotypes (triticum turgidum ssp. Durum) under different environments and water regimes , 2021, Cereal Research Communications.

[3]  K. Nagel,et al.  Deep soil exploration vs. topsoil exploitation: distinctive rooting strategies between wheat landraces and wild relatives , 2020, Plant and Soil.

[4]  J. Le Gouis,et al.  Combining Crop Growth Modeling With Trait-Assisted Prediction Improved the Prediction of Genotype by Environment Interactions , 2020, Frontiers in Plant Science.

[5]  R. Richards,et al.  Root phenotypes of young wheat plants grown in controlled environments show inconsistent correlation with mature root traits in the field , 2020, Journal of experimental botany.

[6]  V. Allard,et al.  Wheat individual grain-size variance originates from crop development and from specific genetic determinism , 2020, PloS one.

[7]  M. Hawkesford,et al.  Functional QTL mapping and genomic prediction of canopy height in wheat measured using a robotic field phenotyping platform , 2020, Journal of experimental botany.

[8]  E. Adeleke,et al.  Variation Analysis of Root System Development in Wheat Seedlings Using Root Phenotyping System , 2020, Agronomy.

[9]  K. Nagel,et al.  Crop Improvement from Phenotyping Roots: Highlights Reveal Expanding Opportunities. , 2019, Trends in plant science.

[10]  F. V. van Eeuwijk,et al.  Using crop growth model stress covariates and AMMI decomposition to better predict genotype-by-environment interactions , 2019, Theoretical and Applied Genetics.

[11]  J. M. Soriano,et al.  Discovering consensus genomic regions in wheat for root-related traits by QTL meta-analysis , 2019, Scientific Reports.

[12]  S. Praud,et al.  Using environmental clustering to identify specific drought tolerance QTLs in bread wheat (T. aestivum L.) , 2019, Theoretical and Applied Genetics.

[13]  W. R. Whalley,et al.  The relationships between seedling root screens, root growth in the field and grain yield for wheat , 2019, Plant and Soil.

[14]  C. Royo,et al.  Genetic Dissection of the Seminal Root System Architecture in Mediterranean Durum Wheat Landraces by Genome-Wide Association Study , 2019, Agronomy.

[15]  C. Doussan,et al.  Scanner-Based Minirhizotrons Help to Highlight Relations between Deep Roots and Yield in Various Wheat Cultivars under Combined Water and Nitrogen Deficit Conditions , 2019, Agronomy.

[16]  A. Hund,et al.  Modern wheat semi-dwarfs root deep on demand: response of rooting depth to drought in a set of Swiss era wheats covering 100 years of breeding , 2019, Euphytica.

[17]  K. Thorup-Kristensen,et al.  Construction of a large-scale semi-field facility to study genotypic differences in deep root growth and resources acquisition , 2019, Plant Methods.

[18]  J. Weiner,et al.  Evolutionary agroecology: Trends in root architecture during wheat breeding , 2018, Evolutionary applications.

[19]  G. Brown-Guedira,et al.  Loci and candidate genes controlling root traits in wheat seedlings—a wheat root GWAS , 2018, Functional & Integrative Genomics.

[20]  G. Fox,et al.  Root architectural traits and yield: exploring the relationship in barley breeding trials , 2018, Euphytica.

[21]  R. Mott,et al.  Functional Mapping of Quantitative Trait Loci (QTLs) Associated With Plant Performance in a Wheat MAGIC Mapping Population , 2018, Front. Plant Sci..

[22]  C. Bastien,et al.  Phenomic Selection Is a Low-Cost and High-Throughput Method Based on Indirect Predictions: Proof of Concept on Wheat and Poplar , 2018, G3: Genes, Genomes, Genetics.

[23]  T. Herben,et al.  Root:shoot ratio in developing seedlings: How seedlings change their allocation in response to seed mass and ambient nutrient supply , 2018, Ecology and evolution.

[24]  Paul H. C. Eilers,et al.  Correcting for spatial heterogeneity in plant breeding experiments with P-splines , 2018 .

[25]  F. Choulet,et al.  Worldwide phylogeography and history of wheat genetic diversity , 2018, Science Advances.

[26]  K. Chenu,et al.  Nitrogen nutrition index predicted by a crop model improves the genomic prediction of grain number for a bread wheat core collection , 2017 .

[27]  D. Sparkes,et al.  Identifying seedling root architectural traits associated with yield and yield components in wheat , 2017, Annals of botany.

[28]  V. Sadras,et al.  Five decades of selection for yield reduced root length density and increased nitrogen uptake per unit root length in Australian wheat varieties , 2016, Plant and Soil.

[29]  Frédéric Cointault,et al.  RhizoTubes as a new tool for high throughput imaging of plant root development and architecture: test, comparison with pot grown plants and validation , 2016, Plant Methods.

[30]  J. Araus,et al.  Interactive effect of water and nitrogen regimes on plant growth, root traits and water status of old and modern durum wheat genotypes , 2016, Planta.

[31]  F. V. van Eeuwijk,et al.  Root phenotyping: from component trait in the lab to breeding. , 2015, Journal of experimental botany.

[32]  M. Kabir,et al.  Mapping QTLs associated with root traits using two different populations in wheat (Triticum aestivum L.) , 2015, Euphytica.

[33]  G. Yan,et al.  Screening Wheat (Triticum spp.) Genotypes for Root Length under Contrasting Water Regimes: Potential Sources of Variability for Drought Resistance Breeding , 2015 .

[34]  Elison B. Blancaflor,et al.  Root Traits and Phenotyping Strategies for Plant Improvement , 2015, Plants.

[35]  H. Mei,et al.  Quantitative trait locus mapping of deep rooting by linkage and association analysis in rice , 2015, Journal of experimental botany.

[36]  Michael P. Pound,et al.  Phenotyping pipeline reveals major seedling root growth QTL in hexaploid wheat , 2015, Journal of experimental botany.

[37]  K. Chenu,et al.  High-throughput phenotyping of seminal root traits in wheat , 2015, Plant Methods.

[38]  K. Eversole,et al.  High throughput SNP discovery and genotyping in hexaploid wheat , 2018, PloS one.

[39]  S. Salvi,et al.  Association mapping for root architectural traits in durum wheat seedlings as related to agronomic performance , 2014, Molecular Breeding.

[40]  V. Ranwez,et al.  Genotyping by sequencing transcriptomes in an evolutionary pre-breeding durum wheat population , 2014, Molecular Breeding.

[41]  S. Praud,et al.  A genome-wide identification of chromosomal regions determining nitrogen use efficiency components in wheat (Triticum aestivum L.) , 2014, Theoretical and Applied Genetics.

[42]  Daowen Wang,et al.  Further genetic analysis of a major quantitative trait locus controlling root length and related traits in common wheat , 2014, Molecular Breeding.

[43]  T. Mahmood,et al.  Relationship between root morphology and grain yield of wheat in north-western NSW, Australia , 2013 .

[44]  R. Richards,et al.  A rapid, controlled-environment seedling root screen for wheat correlates well with rooting depths at vegetative, but not reproductive, stages at two field sites. , 2013, Annals of botany.

[45]  G. Hammer,et al.  QTL for root angle and number in a population developed from bread wheats (Triticum aestivum) with contrasting adaptation to water-limited environments , 2013, Theoretical and Applied Genetics.

[46]  M. Hawkesford,et al.  Identification of QTLs associated with seedling root traits and their correlation with plant height in wheat , 2013, Journal of experimental botany.

[47]  L. Wade,et al.  Genotype x environment interactions for root depth of wheat , 2012 .

[48]  R. Pitman,et al.  Genetic Yield Improvement in Soft Red Winter Wheat in the Eastern United States from 1919 to 2009 , 2012 .

[49]  Bernard Rolland,et al.  A study of genetic progress due to selection reveals a negative effect of climate change on bread wheat yield in France , 2012 .

[50]  J. Lynch,et al.  New roots for agriculture: exploiting the root phenome , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[51]  N. Aparicio,et al.  Genetic improvement of bread wheat yield and associated traits in Spain during the 20th century , 2012, The Journal of Agricultural Science.

[52]  G. Brown-Guedira,et al.  Quantitative Trait Loci Analysis for the Effect of Rht-B1 Dwarfing Gene on Coleoptile Length and Seedling Root Length and Number of Bread Wheat , 2011 .

[53]  P. This,et al.  Novel measures of linkage disequilibrium that correct the bias due to population structure and relatedness , 2011, Heredity.

[54]  G. Rebetzke,et al.  Large root systems: are they useful in adapting wheat to dry environments? , 2011, Functional plant biology : FPB.

[55]  A. Hund,et al.  A consensus map of QTLs controlling the root length of maize , 2011, Plant and Soil.

[56]  J. Lynch,et al.  Shovelomics: high throughput phenotyping of maize (Zea mays L.) root architecture in the field , 2011, Plant and Soil.

[57]  N. Singh,et al.  Relationship of Somatic Cell Count and Mastitis: An Overview , 2011 .

[58]  David Gouache,et al.  Why are wheat yields stagnating in Europe? A comprehensive data analysis for France , 2010 .

[59]  Pierre Martre,et al.  Deviation from the grain protein concentration-grain yield negative relationship is highly correlated to post-anthesis N uptake in winter wheat. , 2010, Journal of experimental botany.

[60]  Y. Benjamini Discovering the false discovery rate , 2010 .

[61]  H. Kang,et al.  Variance component model to account for sample structure in genome-wide association studies , 2010, Nature Genetics.

[62]  Tobias Wojciechowski,et al.  Root phenomics of crops: opportunities and challenges. , 2009, Functional plant biology : FPB.

[63]  Peter J. Gregory,et al.  The effects of dwarfing genes on seedling root growth of wheat , 2009, Journal of experimental botany.

[64]  A. Hund,et al.  Growth of axile and lateral roots of maize: I development of a phenotying platform , 2009, Plant and Soil.

[65]  P. Peltonen-Sainio,et al.  Cereal yield trends in northern European conditions: changes in yield potential and its realisation. , 2009 .

[66]  P. VanRaden,et al.  Efficient methods to compute genomic predictions. , 2008, Journal of dairy science.

[67]  Sébastien Lê,et al.  FactoMineR: An R Package for Multivariate Analysis , 2008 .

[68]  B. Ehdaie,et al.  Domestication and Crop Physiology: Roots of Green-Revolution Wheat , 2007, Annals of botany.

[69]  Jonathan P. Lynch,et al.  Roots of the Second Green Revolution , 2007 .

[70]  Richard Trethowan,et al.  Drought-adaptive traits derived from wheat wild relatives and landraces. , 2006, Journal of Experimental Botany.

[71]  Peter deVoil,et al.  The role of root architectural traits in adaptation of wheat to water-limited environments. , 2006, Functional plant biology : FPB.

[72]  Shawn M. Kaeppler,et al.  Detection of quantitative trait loci for seminal root traits in maize (Zea mays L.) seedlings grown under differential phosphorus levels , 2006, Theoretical and Applied Genetics.

[73]  Loïc Pagès,et al.  Water Uptake by Plant Roots: II – Modelling of Water Transfer in the Soil Root-system with Explicit Account of Flow within the Root System – Comparison with Experiments , 2006, Plant and Soil.

[74]  M. Sorrells,et al.  Association Mapping of Kernel Size and Milling Quality in Wheat (Triticum aestivum L.) Cultivars , 2006, Genetics.

[75]  M. McMullen,et al.  A unified mixed-model method for association mapping that accounts for multiple levels of relatedness , 2006, Nature Genetics.

[76]  W. Thomas,et al.  The effect of semi-dwarf genes on root system size in field-grown barley , 2006, Theoretical and Applied Genetics.

[77]  Edzer J. Pebesma,et al.  Multivariable geostatistics in S: the gstat package , 2004, Comput. Geosci..

[78]  A. G. Bengough,et al.  Gel observation chamber for rapid screening of root traits in cereal seedlings , 2004, Plant and Soil.

[79]  R. Ford Denison,et al.  Darwinian Agriculture: When Can Humans Find Solutions Beyond The Reach of Natural Selection? , 2003, The Quarterly Review of Biology.

[80]  A. Eshel,et al.  Plant Roots : The Hidden Half, Third Edition , 2002 .

[81]  R. Rabbinge,et al.  Comparative response of wheat and oilseed rape to nitrogen supply: absorption and utilisation efficiency of radiation and nitrogen during the reproductive stages determining yield , 2000, Plant and Soil.

[82]  G. Slafer,et al.  CHANGES IN YIELD AND YIELD STABILITY IN WHEAT DURING THE 20TH CENTURY , 1998 .

[83]  A. Oyanagi,et al.  The Direction of Growth of Seminal Roots of Triticum aestivum L. and Experimental Modification Thereof , 1994 .

[84]  R. B. Austin,et al.  Genetic improvement in the yield of winter wheat: a further evaluation , 1989, The Journal of Agricultural Science.

[85]  Betty Klepper,et al.  Quantitative Characterization of Vegetative Development in Small Cereal Grains1 , 1982 .

[86]  J. Waines,et al.  Genetic Variability for Seedling Root Numbers in Wild and Domesticated Wheats 1 , 1979 .

[87]  J. R. Welsh,et al.  Rooting Patterns of Semi‐dwarf and Tall Winter Wheat Cultivars under Dryland Field Conditions 1 , 1977 .

[88]  K. Howse,et al.  Root and shoot growth of semi‐dwarf and taller winter wheats , 1974 .

[89]  C. Donald The breeding of crop ideotypes , 1968, Euphytica.

[90]  W. G. Hill,et al.  Linkage disequilibrium in finite populations , 1968, Theoretical and Applied Genetics.

[91]  J. Garner,et al.  Reanalyses of the historical series of UK variety trials to quantify the contributions of genetic and environmental factors to trends and variability in yield over time , 2010, Theoretical and Applied Genetics.

[92]  Greg J. Rebetzke,et al.  Genetic improvement of early vigour in wheat , 1999 .

[93]  D. Tennant,et al.  Water Use and Water Use Efficiency of Old and Modern Wheat Cultivars in a Mediterranean-type Environment , 1990 .

[94]  R. Richards,et al.  A Breeding Program to Reduce the Diameter of the Major Xylem Vessel in the Seminal Roots of Wheat and its Effect on Grain Yield in Rain-fed Environments , 1989 .

[95]  L O'Brien,et al.  Genetic variability of root growth in wheat (Triticum aestivum L.) , 1979 .

[96]  E. A. Hurd Phenotype and drought tolerance in wheat , 1974 .

[97]  J. Passioura The effect of root geometry on the yield of wheat growing on stored water , 1972 .