麦类遗传育种合辑Triticeae Crops Genetics · Breeding · Germplasm Resources
|Identification of QTL and underlying genes for root system architecture associated with nitrate nutrition in hexaploid wheat
|Marcus GRIFFITHS1, Jonathan A. ATKINSON2, 3, Laura-Jayne GARDINER4, Ranjan SWARUP1, Michael P. POUND5, Michael H. WILSON2, 3, Malcolm J. BENNETT1, 2, 3, Darren M. WELLS1, 2, 3
|1 School of Biosciences, University of Nottingham, Sutton Bonington Campus, LE12 5RD, UK
2 Future Food Beacon of Excellence, University of Nottingham, Sutton Bonington Campus, LE12 5RD, UK
3 Integrative Phenomics Group, School of Biosciences, University of Nottingham, Sutton Bonington Campus, LE12 5RD, UK
4 IBM Research, The Hartree Centre, Warrington, WA4 4AD, UK
5 School of Computer Science, University of Nottingham, Nottingham, NG8 1BB, UK
Abstract The root system architecture (RSA) of a crop has a profound effect on the uptake of nutrients and consequently the potential yield. However, little is known about the genetic basis of RSA and resource adaptive responses in wheat (Triticum aestivum L.). Here, a high-throughput germination paper-based plant phenotyping system was used to identify seedling traits in a wheat doubled haploid mapping population, Savannah×Rialto. Significant genotypic and nitrate-N treatment variation was found across the population for seedling traits with distinct trait grouping for root size-related traits and root distribution-related traits. Quantitative trait locus (QTL) analysis identified a total of 59 seedling trait QTLs. Across two nitrate treatments, 27 root QTLs were specific to the nitrate treatment. Transcriptomic analyses for one of the QTLs on chromosome 2D, which was found under low nitrate conditions, revealed gene enrichment in N-related biological processes and 28 differentially expressed genes with possible involvement in a root angle response. Together, these findings provide genetic insight into root system architecture and plant adaptive responses to nitrate, as well as targets that could help improve N capture in wheat.
Received: 02 December 2020
Accepted: 02 April 2021
|Fund: This work was supported by the Biotechnology and Biological Sciences Research Council, UK (BB/M001806/1, BB/L026848/1, BB/P026834/1, and BB/M019837/1)(MJB, DMW, and MPP); the Leverhulme Trust, UK (RPG-2016–409) (MJB and DMW); the European Research Council FUTUREROOTS Advanced Investigator Grant, UK (294729) to MG, JAA, DMW, and MJB; and the University of Nottingham Future Food Beacon of Excellence, UK.
|About author: Marcus GRIFFITHS, E-mail: email@example.com; Correspondence Darren M. Wells, Tel: +44-115-9516373, E-mail: firstname.lastname@example.org
Cite this article:
Marcus GRIFFITHS, Jonathan A. ATKINSON, Laura-Jayne GARDINER, Ranjan SWARUP, Michael P. POUND, Michael H. WILSON, Malcolm J. BENNETT, Darren M. WELLS.
Identification of QTL and underlying genes for root system architecture associated with nitrate nutrition in hexaploid wheat. Journal of Integrative Agriculture, 21(4): 917-932.
| Akpinar B A, Kantar M, Budak H. 2015. Root precursors of microRNAs in wild emmer and modern wheats show major differences in response to drought stress. Functional & Integrative Genomics, 15, 587–598.
Altschul S F, Gish W, Miller W, Myers E W, Lipman D J. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.
An D, Su J, Liu Q, Zhu Y, Tong Y, Li J, Jing R, Li B, Li Z. 2006. Mapping QTLs for nitrogen uptake in relation to the early growth of wheat (Triticum aestivum L.). Plant and Soil, 284, 73–84.
Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biology, 11, R106.
Antoni R, Dietrich D, Bennett M J, Rodriguez P L. 2016. Hydrotropism: Analysis of the root response to a moisture gradient. Methods in Molecular Biology, 1398, 3–9.
Atkinson J A, Wingen, L U, Griffiths M, Pound M P, Gaju O, Foulkes M J, Le Gouis J, Griffiths S, Bennett M J, King J, Wells D M. 2015. Phenotyping pipeline reveals major seedling root growth QTL in hexaploid wheat. Journal of Experimental Botany, 66, 2283–2292.
Bai C, Liang Y, Hawkesford M J. 2013. Identification of QTLs associated with seedling root traits and their correlation with plant height in wheat. Journal of Experimental Botany, 64, 1745–1753.
Beyer S, Daba S, Tyagi P, Bockelman H, Brown-Guedira G, Mohammadi M. 2019. Loci and candidate genes controlling root traits in wheat seedlings - A wheat root GWAS. Functional & Integrative Genomics, 19, 91–107.
Bolger A M, Lohse M, Usadel B. 2014. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114–2120.
Broman K W, Wu H, Sen Ś, Churchill G A. 2003. R/qtl: QTL mapping in experimental crosses. Bioinformatics, 19, 889–890.
Churchill G A, Doerge R W. 1994. Empirical threshold values for quantitative trait mapping. Genetics, 138, 963–971.
Clark R T, Famoso A N, Zhao K, Shaff J E, Craft E J, Bustamante C D, Mccouch S R, Aneshansley D J, Kochian V. 2013. High-throughput two-dimensional root system phenotyping platform facilitates genetic analysis of root growth and development. Plant, Cell & Environment, 36, 454–466.
Dawson J C, Huggins D R, Jones S S. 2008. Characterizing nitrogen use efficiency in natural and agricultural ecosystems to improve the performance of cereal crops in low-input and organic agricultural systems. Field Crops Research, 107, 89–101.
Delogu G, Cattivelli L, Pecchioni N, De Falcis D, Maggiore T, Stanca A M. 1998. Uptake and agronomic efficiency of nitrogen in winter barley and winter wheat. European Journal of Agronomy, 9, 11–20.
Edgar R C. 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.
El-Gebali S, Mistry J, Bateman A, Eddy S R, Luciani A, Potter S C, Qureshi M, Richardson L J, Salazar G A, Smart A, Sonnhammer E L L, Hirsh L, Paladin L, Piovesan D, Tosatto S C E, Finn R D. 2019. The Pfam protein families database in 2019. Nucleic Acids Research, 47, D427–D432.
Falconer D S. 1996. Introduction to Quantitative Genetics. 4th ed. Longman Group, London.
Fang Z, Xia K, Yang X, Grotemeyer M S, Meier S, Rentsch D, Xu X, Zhang M. 2013. Altered expression of the PTR/NRT1 homologue OsPTR9 affects nitrogen utilization efficiency, growth and grain yield in rice. Plant Biotechnology Journal, 11, 446–458.
FAO (Food and Agriculture Organization of United Nations). 2019. World Fertilizer Trends and Outlook to 2020. Rome, Italy. [2021-02-21]. http://www.fao.org/publications/card/en/c/CA6746EN/
Gaju O, Allard V, Martre P, Snape J W, Heumez E, LeGouis J, Moreau D, Bogard M, Griffiths S, Orford S, Hubbart S, Foulkes M J. 2011. Identification of traits to improve the nitrogen-use efficiency of wheat genotypes. Field Crops Research, 123, 139–152.
Gelli M, Duo Y, Konda A R, Zhang C, Holding D, Dweikat I. 2014. Identification of differentially expressed genes between sorghum genotypes with contrasting nitrogen stress tolerance by genome-wide transcriptional profiling. BMC Genomics, 15, 1–16.
Good A G, Johnson S J, De Pauw M, Carroll R T, Savidov N, Vidmar J, Lu Z, Taylor G, Stroeher V. 2007. Engineering nitrogen use efficiency with alanine aminotransferase. Canadian Journal of Botany, 85, 252–262.
Guo Y, Kong F, Xu Y, Zhao Y, Liang X, Wang Y, An D, Li Si. 2012. QTL mapping for seedling traits in wheat grown under varying concentrations of N, P and K nutrients. Theoretical and Applied Genetics, 124, 851–865.
Habash D Z, Bernard S, Schondelmaier J, Weyen J, Quarrie S A. 2007. The genetics of nitrogen use in hexaploid wheat: N utilisation, development and yield. Theoretical and Applied Genetics, 114, 403–419.
Haley C S, Knott S A. 1992. A simple regression method for mapping quantitative trait loci in line crosses using flanking markers. Heredity, 69, 315–324.
Henderson C R. 1975. Best linear unbiased estimation and prediction under a selection model. Biometrics, 31, 423–444.
Ho C H, Lin S H, Hu H C, Tsay Y F. 2018. CHL1 functions as a nitrate sensor in plants. Cell, 138, 1184–1194.
Hodge A, Berta G, Doussan C, Merchan F, Crespi M. 2009. Plant root growth, architecture and function. Plant and Soil, 321, 153–187.
Huang N C, Liu K H, Lo H J, Tsay Y F. 1999. Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low-affinity uptake. Plant Cell, 11, 1381–1392.
Husson F, Josse J, Le S, Maintainer J M. 2019. R Package “FactoMineR”: Multivariate exploratory data analysis and data mining. [2019-08-05]. https://github.com/husson/FactoMineR
IWGSC (International Wheat Genome Sequencing Consortium). 2018. Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science, 361, eaar7191.
Kanno Y, Hanada A, Chiba Y, Ichikawa T, Nakazawa M, Matsui M, Koshiba T, Kamiya Y, Seo M. 2012. Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor. Proceedings of the National Academy of Sciences of the United States of America, 109, 9653–9658.
Kant S, Bi Y M, Rothstein S J. 2011. Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency. Journal of Experimental Botany, 62, 1499–1509.
Kawahara Y, de la Bastide M, Hamilton J P, Kanamori H, Mccombie W R, Ouyang S, Schwartz D C, Tanaka T, Wu J, Zhou S, Childs K L, Davidson R M, Lin H, Quesada-Ocampo L, Vaillancourt B, Sakai H, Lee S S, Kim J, Numa H, Itoh T, et al. 2013. Improvement of the Oryza sativa nipponbare reference genome using next generation sequence and optical map data. Rice, 6, 3–10.
Krogh A, Larsson B, Von Heijne G, Sonnhammer E L L. 2001. Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. Journal of Molecular Biology, 305, 567–580.
Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K, Mounier E, Hoyerova K, Tillard P, Leon S, Ljung K, Zazimalova E, Benkova E, Nacry P, Gojon A. 2010. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Developmental Cell, 18, 927–937.
Kuznetsova A, Brockhoff P B, Christensen R H B. 2017. lmerTest package: Tests in linear mixed effects models. Journal of Statistical Software, 82 1–26.
Landjeva S, Neumann K, Lohwasser U, Börner A. 2008. Molecular mapping of genomic regions associated with wheat seedling growth under osmotic stress. Plant Biology, 52, 259–266.
Lark R M, Milne A E, Addiscott T M, Goulding K W T, Webster C P, O’Flaherty S. 2004. Scale- and location-dependent correlation of nitrous oxide emissions with soil properties: An analysis using wavelets. European Journal of Soil Science, 55, 611–627.
Léran S, Varala K, Boyer J C, Chiurazzi M, Crawford N, Daniel-Vedele F, David L, Dickstein R, Fernandez E, Forde B, Gassmann W, Geiger D, Gojon A, Gong J M, Halkier B A, Harris J M, Hedrich R, Limami A M, Rentsch D, Seo M, et al. 2014. A unified nomenclature of nitrate transporter 1/peptide transporter family members in plants. Trends in Plant Science, 19, 5–9.
Liu X, Li R, Chang X, Jing R. 2013. Mapping QTLs for seedling root traits in a doubled haploid wheat population under different water regimes. Euphytica, 189, 51–66.
Lobet G, Pound M P, Diener J, Pradal C, Draye X, Godin C, Javaux M, Leitner D, Meunier F, Nacry P, Pridmore T P, Schnepf A. 2015. Root system markup language: Toward a unified root architecture description language. Plant Physiology, 167, 617–627.
Miller A J, Fan X, Orsel M, Smith S J, Wells D M. 2007. Nitrate transport and signalling. Journal of Experimental Botany, 58, 2297–2306.
Mooney S J, Pridmore T P, Helliwell J, Bennett M J. 2012. Developing X-ray computed tomography to non-invasively image 3-D root systems architecture in soil. Plant and Soil, 352, 1–22.
Oono Y, Kawahara Y, Yazawa T, Kanamori H, Kuramata M, Yamagata H, Hosokawa S, Minami H, Ishikawa S, Wu J, Antonio B, Handa H, Itoh T, Matsumoto T. 2013. Diversity in the complexity of phosphate starvation transcriptomes among rice cultivars based on RNA-Seq profiles. Plant Molecular Biology, 83, 523–537.
Ouellette L A, Reid R W, Blanchard S G, Brouwer C R. 2018. LinkageMapView-rendering high-resolution linkage and QTL maps. Bioinformatics, 34, 306–307.
Pertea M, Kim D, Pertea G M, Leek J T, Salzberg S L. 2016. RNA-seq experiments with HISAT, StringTie and Ballgown. Nature Protocols, 11, 1650–1667.
Pound M P, French A P, Atkinson J A, Wells D M, Bennett M J, Pridmore T. 2013. RootNav: Navigating images of complex root architectures. Plant Physiology, 162, 1802–1814.
Raudvere U, Kolberg L, Kuzmin I, Arak T, Adler P, Peterson H, Vilo J. 2019. g:Profiler: A web server for functional enrichment analysis and conversions of gene lists 2019 update. Nucleic Acids Research, 47, W191–W198.
Remans T, Nacry P, Pervent M, Filleur S, Diatloff E, Mounier E, Tillard P, Forde B G, Gojon A. 2006. The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proceedings of the National Academy of Sciences of the United States of America, 103, 19206–19211.
Ren Y, He X, Liu D, Li J, Zhao X, Li B, Tong Y, Zhang A, Li Z. 2012. Major quantitative trait loci for seminal root morphology of wheat seedlings. Molecular Breeding, 30, 139–148.
Rich S M, Christopher J, Richards R, Watt M. 2020. Root phenotypes of young wheat plants grown in controlled environments show inconsistent correlation with mature root traits in the field. Journal of Experimental Botany, 71, 4751–4762.
Roselló M, Royo C, Sanchez-Garcia M, Soriano J M. 2019. Genetic dissection of the seminal root system architecture in Mediterranean durum wheat landraces by genome-wide association study. Agronomy, 9, 364.
Schindelin J, Arganda-Carrera I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez J V, White D J, Hartenstein V, Eliceiri K, Tomancak P, Cardona A. 2012. Fiji: An open-source platform for biological-image analysis. Nature Methods, 9, 676–682.
Stamatakis A. 2014. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313.
Sun J, Guo Y, Zhang G, Gao M, Zhang G, Kong F, Zhao Y, Li S. 2013. QTL mapping for seedling traits under different nitrogen forms in wheat. Euphytica, 191, 317–331.
Takahashi N, Goto N, Okada K, Takahashi H. 2002. Hydrotropism in abscisic acid, wavy, and gravitropic mutants of Arabidopsis thaliana. Planta, 216, 203–211.
Trachsel S, Kaeppler S M, Brown K M, Lynch J P. 2013. Maize root growth angles become steeper under low N conditions. Field Crops Research, 140, 18–31.
Wang S, Wong D, Forrest K, Allen A, Chao S, Huang B E, Maccaferri M, Salvi S, Milner S G, Cattivelli L, Mastrangelo A M, Whan A, Stephen S, Barker G, Wieseke R, Plieske J, International Wheat Genome Sequencing Consortium, Lillemo M, Mather D, Appels R. 2014. Characterization of polyploid wheat genomic diversity using a high-density 90 000 single nucleotide polymorphism array. Plant Biotechnology Journal, 12, 787–796.
Watt M, Moosavi S, Cunningham S C, Kirkegaard J A, Rebetzke G J, Richards R A. 2013. A rapid, controlled-environment seedling root screen for wheat correlates well with rooting depths at vegetative, but not reproductive, stages at two field sites. Annals of Botany, 112, 447–455.
Wei T, Simko V. 2017. R package ‘corrplot’: Visualization of a CORRELATION Matrix. version 0.84. [2020-07-28]. https://github.com/taiyun/corrplot
Xu C, Zhang H, Sun J, Guo Z, Zou C, Li W X, Xie C, Huang C, Xu R, Liao H, Wang J, Xu X, Wang S, Xu Y. 2018. Genome-wide association study dissects yield components associated with low-phosphorus stress tolerance in maize. Theoretical and Applied Genetics, 131, 1699–1714.
Yang M, Wang C R, Hassan M A, Wu Y Y, Xia X. 2020. QTL mapping of seedling biomass and root traits under different nitrogen conditions in bread wheat (Triticum aestivum L.). Journal of Integrative Agriculture, 19, 2–14.
Yu G, Smith D K, Zhu H, Guan Y, Lam T T Y. 2017. Ggtree: An R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods in Ecology and Evolution, 8, 28–36.
Yu P, Eggert K, von Wirén N, Li C, Hochholdinger F. 2015. Cell type-specific gene expression analyses by RNA sequencing reveal local high nitrate-triggered lateral root initiation in shoot-borne roots of maize by modulating auxin-related cell cycle regulation. Plant Physiology, 169, 690–704.
Zhang H, Cui F, Wang L, Li J, Ding A, Zhao C, Bao Y, Yang Q, Wang H. 2013. Conditional and unconditional QTL mapping of drought-tolerance-related traits of wheat seedling using two related RIL populations. Journal of Genetics, 92, 213–231.
Zimin A V, Marçais G, Puiu D, Roberts M, Salzberg S L, Yorke J A. 2013. The MaSuRCA genome assembler. Bioinformatics, 29, 2669–2677.
Zurek P R, Topp C N, Benfey P N. 2015. Quantitative trait locus mapping reveals regions of the maize genome controlling root system architecture. Plant Physiology, 167, 1487–1496.
|No Suggested Reading articles found!