Linking root length and surface area to yield: variety-specific root plasticity in winter wheat across contrasting European environments
Jazyk angličtina Země Velká Británie, Anglie Médium print
Typ dokumentu časopisecké články
Grantová podpora
EJP Soil
862695
European Union's Horizon 2020 Research and Innovation Programme
Horizon 2020
817970
European Union's Horizon 2020 Framework Programme
PubMed
40668186
PubMed Central
PMC12682866
DOI
10.1093/aob/mcaf155
PII: 8203343
Knihovny.cz E-zdroje
- Klíčová slova
- Triticum aestivum L, EJP Soil, deep-rooting, heritability, management, pedoclimatic gradient, root length, root plasticity, root surface area, soil, winter wheat, yield,
- MeSH
- klimatické změny MeSH
- kořeny rostlin * růst a vývoj anatomie a histologie fyziologie MeSH
- podnebí MeSH
- pšenice * růst a vývoj anatomie a histologie fyziologie MeSH
- půda chemie MeSH
- roční období MeSH
- životní prostředí MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Evropa MeSH
- Názvy látek
- půda MeSH
BACKGROUND AND AIMS: Understanding the relationship of root traits and crop performance under varying environmental conditions facilitates the exploitation of root characteristics in breeding and variety testing to maintain crop yields under climate change. Therefore, we (1) evaluated differences in root length and surface area between ten winter wheat varieties grown at 11 sites in Europe covering a large pedoclimatic gradient, (2) quantified differences in root response to soil, climate and management conditions between varieties, and (3) evaluated variety-specific relationships of grain yield and root length and surface area under diverse environmental conditions. METHODS: At each site, we sampled the roots to 1 m soil depth after harvest and determined various root traits by scanning and image analysis. The impacts of soil, climate and management on roots and yield of the ten varieties were analysed by means of multivariate mixed models. KEY RESULTS: Root length averaged 1.4 m root piece-1, 5007 m root m-2 soil, and 5300 m root m-2 soil and root surface area 0.039 m2 root piece-1, 40 m2 root m-2 soil, and 43 m2 root m-2 soil in 0.00-0.15 m, 0.15-0.50 m, 0.50-1.00 m soil depth, respectively. The variation in both traits was 10 times higher between sites than varieties, the latter ranging by a factor of 2 within sites. Irrespective of variety, temperature was a major driver of subsoil root traits, suggesting that warmer climates promoted root growth in deeper soil layers. Other soil and climate variables affected root length and/or root surface area of individual varieties, highlighting different degrees of root plasticity. The varieties displayed distinctly different relationships between yield and root traits under varying pedoclimatic conditions, highlighting genetic differences in yield response to environmentally driven root plasticity. CONCLUSIONS: These findings suggest that breeding efforts should target flexible root-yield relationships in the subsoil to maintain crop performance under climate change.
Agroscope Agroecology and Environment Soil Quality and Soil Use 8046 Zurich Switzerland
Austrian Agency for Health and Food Safety Seed Seedling and Variety Assessment 1220 Vienna Austria
ETH Zurich Institute of Agricultural Sciences 8092 Zurich Switzerland
National Food Chain Safety Office Agricultural Genetic Resources Directorate 1024 Budapest Hungary
Norwegian Institute of Bioeconomy Research Biogeochemistry and Soil Quality 1430 Ås Norway
Technical University Munich School of Life Sciences Precision Agriculture Lab 85354 Freising Germany
Thünen Institute Institute of Climate Smart Agriculture 38116 Braunschweig Germany
Walloon Agricultural Research Centre Crop Production Unit 5030 Gembloux Belgium
Zobrazit více v PubMed
York LM. Plans for root scanning trays to use on flatbed scanners. Zenodo. 2020. doi: 10.5281/zenodo.4122423. DOI
Addy JWG, Ellis RH, MacLaren C, Macdonald AJ, Semenov MA, Mead A. 2022. A heteroskedastic model of park grass spring hay yields in response to weather suggests continuing yield decline with climate change in future decades. Journal of the Royal Society Interface 19: 20220361. PubMed PMC
Adeleke E, Millas R, McNeal W, Faris J, Taheri A. 2020. Variation analysis of root system development in wheat seedlings using root phenotyping system. Agronomy 10: 206.
Agnolucci P, De Lipsis V. 2020. Long-run trend in agricultural yield and climatic factors in Europe. Climatic Change 159: 385–405.
Agrarmeteorologisches Messnetz Sachsen .
Agrometeo . 2024.
Aiken LS, West SG. 1991. Multiple regression: testing and interpreting interactions, Vol. 2. Newbury Park, CA: Sage Publications.
Ajjur SB, Al-Ghamdi SG. 2021. Evapotranspiration and water availability response to climate change in the Middle East and North Africa. Climatic Change 166: 28.
Akman H. 2020. Comparison of field crops with tap and fibrous root system at early and late growth stages. Turkish Journal of Agriculture – Food Science and Technology 8: 1181–1187.
Alahmad S, El Hassouni K, Bassi FM, et al. 2019. A major root architecture QTL responding to water limitation in durum wheat. Frontiers in Plant Science 10: 436. PubMed PMC
International Wheat Genome Sequencing Consortium (IWGSC), Appels R, Eversole K, et al. 2018. Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361: eaar7191. PubMed
Asseng S, Ritchie JT, Smucker AJM, Robertson MJ. 1998. Root growth and water uptake during water deficit and recovering in wheat. Plant and Soil 201: 265–273.
Bartoń K. 2023.
Bates D, Maechler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67: 1–48.
Bayerisches Landesamt für Umwelt .
Bengough AG, McKenzie BM, Hallett PD, Valentine TA. 2011. Root elongation, water stress, and mechanical impedance: a review of limiting stresses and beneficial root tip traits. Journal of Experimental Botany 62: 59–68. PubMed
Biecek P. 2018. DALEX: explainers for complex predictive models in R. Journal of Machine Learning Research 19: 1–5.
Brás TA, Seixas J, Carvalhais N, Jägermeyr J. 2021. Severity of drought and heatwave crop losses tripled over the last five decades in Europe. Environmental Research Letters 16: 065012.
Calleja Cabrera J, Boter M, Oñate-Sánchez L, Pernas M. 2020. Root growth adaptation to climate change in crops. Frontiers in Plant Science 11: 544. PubMed PMC
Chaves MM, Pereira JS, Maroco J, et al. 2002. How plants cope with water stress in the field. Photosynthesis and growth. Annals of Botany 89: 907–916. PubMed PMC
Chen H, Wei J, Tian R, et al. 2022. A major quantitative trait locus for wheat total root length associated with precipitation distribution. Frontiers in Plant Science 13: 995183. PubMed PMC
Colombo M, Roumet P, Salon C, et al. 2022. Genetic analysis of platform-phenotyped root system architecture of bread and durum wheat in relation to agronomic traits. Frontiers in Plant Science 13: 853601. PubMed PMC
Correa J, Postma JA, Watt M, Wojciechowski T. 2019. Soil compaction and the architectural plasticity of root systems. Journal of Experimental Botany 70: 6019–6034. PubMed PMC
Dinneny JR. 2019. Developmental responses to water and salinity in root systems. Annual Review of Cell and Developmental Biology 35: 239–257. PubMed
Doolittle JA, Brevik EC. 2014. The use of electromagnetic induction techniques in soils studies. Geoderma 223: 33–45.
Duan D, Feng X, Wu N, et al. 2023. Drought eliminates the difference in root trait plasticity and mycorrhizal responsiveness of two semiarid grassland species with contrasting root system. International Journal of Molecular Sciences 24: 10262. PubMed PMC
EUPVP – EU Plant Variety Portal . 2023.
European Environment Agency . 2017. Biogeographical regions in Europe.
FAO .
Federal Office of Meteorology and Climatology MeteoSwiss .
Fox J, Weisberg S. 2019.
Fradgley N, Evans G, Biernaskie JM, et al. 2020. Effects of breeding history and crop management on the root architecture of wheat. Plant and Soil 452: 587–600. PubMed PMC
Frasier I, Noellemeyer E, Fernandez R, Quiroga A. 2016. Direct field method for root biomass quantification in agroecosystems. MethodsX 3: 513–519. PubMed PMC
Fry EL, Evans AL, Sturrock CJ, Bullock JM, Bardgett RD. 2018. Root architecture governs plasticity in response to drought. Plant and Soil 433: 189–200. PubMed PMC
Gauch HG, Qian S, Piepho H-P, Zhou L, Chen R. 2019. Consequences of PCA graphs, SNP codings, and PCA variants for elucidating population structure. PLoS One 14: e0218306. PubMed PMC
GeoSphere Austria . 2023. DOI
Giorgi F, Bi X, Pal J. 2004. Mean, interannual variability and trends in a regional climate change experiment over Europe. II: climate change scenarios (2071–2100). Climate Dynamics 23: 839–858.
Gogna A, Schulthess AW, Röder MS, Ganal MW, Reif JC. 2022. Gabi wheat a panel of European elite lines as central stock for wheat genetic research. Scientific Data 9: 538. PubMed PMC
Gowda VRP, Henry A, Yamauchi A, Shashidhar HE, Serraj R. 2011. Root biology and genetic improvement for drought avoidance in rice. Field Crops Research 122: 1–13.
Goyal RK. 2004. Sensitivity of evapotranspiration to global warming: a case study of arid zone of Rajasthan (India). Agricultural Water Management 69: 1–11.
Gregory PJ. 2006. Roots and the architecture of root systems. In: Gregory PJ. ed. Plant roots: growth, activity and interactions with the soil. Oxford: Wiley-Blackwell, 18–44.
Grossman JD, Rice KJ. 2012. Evolution of root plasticity responses to variation in soil nutrient distribution and concentration. Evolutionary Applications 5: 850–857. PubMed PMC
Gulino D, Sayeras R, Serra J, et al. 2023. Impact of rising temperatures on historical wheat yield, phenology, and grain size in Catalonia Frontiers in Plant Science 14: 1245362. PubMed PMC
Guo H, Ayalew H, Seethepalli A, et al. 2021. Functional phenomics and genetics of the root economics space in winter wheat using high-throughput phenotyping of respiration and architecture. New Phytologist 232: 98–112. PubMed PMC
Guo X, Svane SF, Füchtbauer WS, Andersen JR, Jensen J, Thorup-Kristensen K. 2020. Genomic prediction of yield and root development in wheat under changing water availability. Plant Methods 16: 90. PubMed PMC
Hashemi M, Schneider K. 2020.
Hecht VL, Temperton VM, Nagel KA, Rascher U, Postma JA. 2016. Sowing density: a neglected factor fundamentally affecting root distribution and biomass allocation of field grown spring barley ( PubMed PMC
Heinemann H, Durand-Maniclas F, Seidel F, et al. 2025. Optimising root and grain yield through variety selection in winter wheat across a European climate gradient. European Journal of Soil Science 76: e70077.
Heinemann H, Hirte J, Seidel F, Don A. 2023. Increasing root biomass derived carbon input to agricultural soils by genotype selection – a review. Plant and Soil 490: 19–30.
Hirte J, Leifeld J, Abiven S, Mayer J. 2018. Maize and wheat root biomass, vertical distribution, and size class as affected by fertilization intensity in two long-term field trials. Field Crops Research 216: 197–208.
Hirte J, Walder F, Hess J, et al. 2021. Enhanced root carbon allocation through organic farming is restricted to topsoils. Science of the Total Environment 755: 143551. PubMed
Hochholdinger F, Tuberosa R. 2009. Genetic and genomic dissection of maize root development and architecture. Current Opinion in Plant Biology 12: 172–177. PubMed
Hothorn T, Bretz F, Westfall P. 2008. Simultaneous inference in general parametric models. Biometrical Journal_ 50: 346–363. PubMed
Hund A, Richner W, Soldati A, Fracheboud Y, Stamp P. 2007. Root morphology and photosynthetic performance of maize inbred lines at low temperature. European Journal of Agronomy 27: 52–61.
Karlova R, Boer D, Hayes S, Testerink C. 2021. Root plasticity under abiotic stress. Plant Physiology 187: 1057–1070. PubMed PMC
Kassambara A. 2023.
Kell DB. 2011. Breeding crop plants with deep roots: their role in sustainable carbon, nutrient and water sequestration. Annals of Botany 108: 407–418. PubMed PMC
Khan MA, Gemenet DC, Villordon A. 2016. Root system architecture and abiotic stress tolerance: current knowledge in root and tuber crops. Frontiers in Plant Science 7: 1584. PubMed PMC
Kirkegaard JA, Lilley JM, Howe GN, Graham JM. 2007. Impact of subsoil water use on wheat yield. Australian Journal of Agricultural Research 58: 303–315.
Koevoets IT, Venema JH, Elzenga JTM, Testerink C. 2016. Roots withstanding their environment: exploiting root system architecture responses to abiotic stress to improve crop tolerance. Frontiers in Plant Science 7: 1335. PubMed PMC
Kolb E, Legué V, Bogeat-Triboulot M-B. 2017. Physical root–soil interactions. Physical Biology 14: 065004. PubMed
Le Gouis J, Oury F-X, Charmet G. 2020. How changes in climate and agricultural practices influenced wheat production in Western Europe. Journal of Cereal Science 93: 102960.
Lenth R. 2023.
Li X, Ingvordsen CH, Weiss M, et al. 2019. Deeper roots associated with cooler canopies, higher normalized difference vegetation index, and greater yield in three wheat populations grown on stored soil water. Journal of Experimental Botany 70: 4963–4974. PubMed PMC
Li C, Li L, Reynolds MP, et al. 2021. Recognizing the hidden half in wheat: root system attributes associated with drought tolerance. Journal of Experimental Botany 72: 5117–5133. PubMed
Liaw A, Wiener M. 2002. Classification and regression by randomForest. R News 2: 18–22.
Lipiec J, Horn R, Pietrusiewicz J, Siczek A. 2012. Effects of soil compaction on root elongation and anatomy of different cereal plant species. Soil and Tillage Research 121: 74–81.
Lithuanian Hydrometeorological Service . 2022.
Liu J, Liu Y, Wang S, Cui Y, Yan D. 2022. Heat stress reduces root meristem size via induction of plasmodesmal callose accumulation inhibiting phloem unloading in PubMed PMC
Livesley SJ, Stacey CL, Gregory PJ, Buresh RJ. 1999. Sieve size effects on root length and biomass measurements of maize (
Lobell DB, Schlenker W, Costa-Roberts J. 2011. Climate trends and global crop production since 1980. Science 333: 616–620. PubMed
Lopes MS. 2022. Will temperature and rainfall changes prevent yield progress in Europe? Food and Energy Security 11: e372.
Lopes MS, Reynolds MP. 2010. Partitioning of assimilates to deeper roots is associated with cooler canopies and increased yield under drought in wheat. Functional Plant Biology 37: 147–156.
Lozano-Isla F. 2023.
Lüdeke D. 2023.
Lüdeke D. 2018. Sjmisc: data and variable transformation functions. Journal of Open Source Software 3: 754.
Luo DG, Ganesh S, Koolaard J. 2022.
Lynch J. 1995. Root architecture and plant productivity. Plant Physiology 109: 7–13. PubMed PMC
Lynch JP. 2013. Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Annals of Botany 112: 347–357. PubMed PMC
Lynch JP. 2018. Rightsizing root phenotypes for drought resistance. Journal of Experimental Botany 69: 3279–3292. PubMed
Lynch JP, Wojciechowski T. 2015. Opportunities and challenges in the subsoil: pathways to deeper rooted crops. Journal of Experimental Botany 66: 2199–2210. PubMed PMC
Madsen H, Lawrence D, Lang M, Martinkova M, Kjeldsen TR. 2014. Review of trend analysis and climate change projections of extreme precipitation and floods in Europe. Journal of Hydrology 519: 3634–3650.
Maqbool S, Hassan MA, Xia X, York LM, Rasheed A, He Z. 2022. Root system architecture in cereals: progress, challenges and perspective. Plant Journal 110: 23–42. PubMed
Mathew I, Shimelis H. 2022. Genetic analyses of root traits: implications for environmental adaptation and new variety development: a review. Plant Breeding 141: 695–718.
Mathew I, Shimelis H, Shayanowako AIT, Laing M, Chaplot V. 2019. Genome-wide association study of drought tolerance and biomass allocation in wheat. PLoS One 14: e0225383. PubMed PMC
Merotto A, Mundstock CM. 1999. Wheat root growth as affected by soil strength. Revista Brasileira de Ciencia do Solo 23: 197–202.
Monyo JH, Whittington WJ. 1970. Genetic analysis of root growth in wheat. Journal of Agricultural Science 74: 329–338.
Mooney SJ, Pridmore TP, Helliwell J, Bennett MJ. 2012. Developing X-ray computed tomography to non-invasively image 3-D root systems architecture in soil. Plant and Soil 352: 1–22.
Moore FC, Lobell DB. 2015. The fingerprint of climate trends on European crop yields. Proceedings of the National Academy of Sciences of the United States of America 112: 2670–2675. PubMed PMC
Nelson GC, Cheung WWL, Bezner Kerr R, et al. 2024. Adaptation to climate change and limits in food production systems: physics, the chemistry of biology, and human behavior. Global Change Biology 30: e17489. PubMed
Ober ES, Alahmad S, Cockram J, et al. 2021. Wheat root systems as a breeding target for climate resilience. Theoretical and Applied Genetics 134: 1645–1662. PubMed PMC
Odone A, Popovic O, Thorup-Kristensen K. 2023. Deep roots: implications for nitrogen uptake and drought tolerance among winter wheat cultivars. Plant and Soil 500: 13–32.
Oldenbroek K, van der Waaij L. 2015. Textbook animal breeding and genetics for BSc students. Wageningen, The Netherlands: Centre for Genetic Resources, The Netherlands and Animal Breeding and Genomics Centre.
Olsen SR. 1954. Estimation of available phosphorus in soils by extraction with sodium bicarbonate. Washington, DC: US Department of Agriculture.
Osmont KS, Sibout R, Hardtke CS. 2007. Hidden branches: developments in root system architecture. Annual Review of Plant Biology 58: 93–113. PubMed
Pariyar SR, Nagel KA, Lentz J, et al. 2021. Variation in root system architecture among the founder parents of two 8-way MAGIC wheat populations for selection in breeding. Agronomy 11: 2452.
Paustian K, Lehmann J, Ogle S, Reay D, Robertson GP, Smith P. 2016. Climate-smart soils. Nature 532: 49–57. PubMed
Piepho H-P, Möhring J. 2007. Computing heritability and selection response from unbalanced plant breeding trials. Genetics 177: 1881–1888. PubMed PMC
Pierret A, Moran CJ, Doussan C. 2005. Conventional detection methodology is limiting our ability to understand the roles and functions of fine roots. New Phytologist 166: 967–980. PubMed
Pinheiro J, Bates D. 2006. Mixed-effects models in S and S-PLUS. New York, NY: Springer.
Pinheiro JB, Bates D, R Core Team . 2023.
Porter JR, Gawith M. 1999. Temperatures and the growth and development of wheat: a review. European Journal of Agronomy 10: 23–36.
Qi F, Zhang F. 2020. Cell cycle regulation in the plant response to stress. Frontiers in Plant Science 10: 1765. PubMed PMC
Raffo MA, Jensen J. 2023. Gene × gene and genotype × environment interactions in wheat. Crop Science 63: 1779–1793.
Rasse DP. 2002. Nitrogen deposition and atmospheric CO
Rasse DP, Smucker AJM. 1998. Root recolonization of previous root channels in corn and alfalfa rotations. Plant and Soil 204: 203–212.
R Core Team . 2023.
Ribeiro PR, Fernandez LG, de Castro RD, Ligterink W, Hilhorst HWM. 2014. Physiological and biochemical responses of PubMed PMC
Rich SM, Watt M. 2013. Soil conditions and cereal root system architecture: review and considerations for linking Darwin and Weaver. Journal of Experimental Botany 64: 1193–1208. PubMed
RMI, Royal Meteorological Institute of Belgium .
Rogers ED, Benfey PN. 2015. Regulation of plant root system architecture: implications for crop advancement. Current Opinion in Biotechnology 32: 93–98. PubMed
Samset BH, Zhou C, Fuglestvedt JS, Lund MT, Marotzke J, Zelinka MD. 2023. Steady global surface warming from 1973 to 2022 but increased warming rate after 1990. Communications Earth & Environment 4: 400.
Sandhu N, Raman KA, Torres RO, et al. 2016. Rice root architectural plasticity traits and genetic regions for adaptability to variable. Cultivation and Stress Conditions Plant Physiology 171: 2562–2576. PubMed PMC
Schneider HM, Lynch JP. 2020. Should root plasticity be a crop breeding target? Frontiers in Plant Science 11: 546. PubMed PMC
Seethepalli A, Dhakal K, Griffiths M, Guo H, Freschet GT, York LM. 2021. RhizoVision explorer: open-source software for root image analysis and measurement standardization. AoB Plants 13: plab056. PubMed PMC
Seethepalli A, York LM. 2021.
Severini AD, Wasson AP, Evans JR, Richards RA, Watt M. 2020. Root phenotypes at maturity in diverse wheat and triticale genotypes grown in three field experiments: relationships to shoot selection, biomass, grain yield, flowering time, and environment. Field Crops Research 255: 107870.
Shenoy A. 2021. grafify: an R package for easy graphs, ANOVAs and post-hoc comparisons. Version 4.0. doi: 10.5281/zenodo.5136508 (31 March 2024, date last accessed). DOI
Shewry PR, Hey SJ. 2015. The contribution of wheat to human diet and health. Food and Energy Security 4: 178–202. PubMed PMC
Shoaib M, Banerjee BP, Hayden M, Kant S. 2022. Roots’ drought adaptive traits in crop improvement. Plants (Basel) 11: 2256. PubMed PMC
Siddique KHM, Kirby EJM, Perry MW. 1989. Ear: stem ratio in old and modern wheat varieties; relationship with improvement in number of grains per ear and yield. Field Crops Research 21: 59–78.
Smith S, De Smet I. 2012. Root system architecture: insights from PubMed PMC
Smucker AJM, McBurney SL, Srivastava AK. 1982. Quantitative separation of roots from compacted soil profiles by the hydropneumatic elutriation system. Agronomy Journal 74: 500–503.
Solomon S, Qin D, Manning M et al. 2007. IPCC, 2007: climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change, Vol. 4. Cambridge: Cambridge University Press.
Sun X, Wang P, Mi G. 2025. Genotypic differences in maize root morphology in response to low-nitrogen stress. Agronomy 15: 332.
Svoboda P, Kurešová G, Raimanová I, Kunzová E, Haberle J. 2020. The effect of different fertilization treatments on wheat root depth and length density distribution in a long-term experiment. Agronomy 10: 1355.
Timaeus J, Weedon OD, Finckh MR. 2021. Combining genetic gain and diversity in plant breeding: heritability of root selection in wheat populations. Sustainability 13: 12778.
Trachsel S, Kaeppler SM, Brown KM, Lynch JP. 2011. Shovelomics: high throughput phenotyping of maize (
Tripathy KP, Mishra AK. 2023. How unusual is the 2022 European Compound Drought and Heatwave event? Geophysical Research Letters 50: e2023GL105453.
Uga Y. 2021. Challenges to design-oriented breeding of root system architecture adapted to climate change. Breeding Science 71: 3–12. PubMed PMC
Vu V. 2011.
Vu LD, Gevaert K, De Smet I. 2019. Feeling the heat: searching for plant thermosensors. Trends in Plant Science 24: 210–219. PubMed
Whalley WR, Binley A, Watts CW, et al. 2017. Methods to estimate changes in soil water for phenotyping root activity in the field. Plant and Soil 415: 407–422. PubMed PMC
Whalley WR, Leeds-Harrison PB, Clark LJ, Gowing DJG. 2005. Use of effective stress to predict the penetrometer resistance of unsaturated agricultural soils. Soil & Tillage Research 84: 18–27.
Wickham H. 2007. Reshaping data with the reshape package. Journal of Statistical Software 21: 1–20.
Wickham H. 2016. Ggplot2: elegant graphics for data analysis. New York: Springer.
Wickham H, Averick M, Bryan J, et al. 2019. Welcome to the tidyverse. Journal of Open Source Software 4: 1686.
Wickham H, Bryan J. 2023.
Wickham H, Seidel D.
World Reference Base . 2014. World reference base for soil resources 2014. International soil classification system for naming soils and creating legends for soil maps, Vol. 106. Rome, Italy: Food and Agriculture Organization of the United Nations (FAO).
World Reference Base . 2022. World reference base for soil resources. International soil classification system for naming soils and creating legends for soil maps, Vol. 4. Vienna, Austria: International Union of Soil Sciences (IUSS).
Xie Q, Fernando KMC, Mayes S, Sparkes DL. 2017. Identifying seedling root architectural traits associated with yield and yield components in wheat. Annals of Botany 119: 1115–1129. PubMed PMC
Xie X, Quintana MR, Sandhu N, et al. 2021. Establishment method affects rice root plasticity in response to drought and its relationship with grain yield stability. Journal of Experimental Botany 72: 5208–5220. PubMed
Xu F, Chen S, Yang X, et al. 2021. Genome-wide association study on root traits under different growing environments in wheat ( PubMed PMC
Yang J-C, Zhang H, Zhang J-H. 2012. Root morphology and physiology in relation to the yield formation of rice. Journal of Integrative Agriculture: JIA 11: 920–926.
Zhang Z, Murtagh F, Van Poucke S, Lin S, Lan P. 2017. Hierarchical cluster analysis in clinical research with heterogeneous study population: highlighting its visualization with R. Annals of Translational Medicine 5: 75. PubMed PMC