Skip to main content

Advertisement

SpringerLink
Log in

Genomic basis determining root system architecture in maize

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

A total of 389 and 344 QTLs were identified by GWAS and QTL mapping explaining accumulatively 32.2–65.0% and 23.7–63.4% of phenotypic variation for 14 shoot-borne root traits using more than 1300 individuals across multiple field trails.

Abstract

Efficient nutrient and water acquisition from soils depends on the root system architecture (RSA). However, the genetic determinants underlying RSA in maize remain largely unexplored. In this study, we conducted a comprehensive genetic analysis for 14 shoot-borne root traits using 513 inbred lines and 800 individuals from four recombinant inbred line (RIL) populations at the mature stage across multiple field trails. Our analysis revealed substantial phenotypic variation for these 14 root traits, with a total of 389 and 344 QTLs identified through genome-wide association analysis (GWAS) and linkage analysis, respectively. These QTLs collectively explained 32.2–65.0% and 23.7–63.4% of the trait variation within each population. Several a priori candidate genes involved in auxin and cytokinin signaling pathways, such as IAA26, ARF2, LBD37 and CKX3, were found to co-localize with these loci. In addition, a total of 69 transcription factors (TFs) from 27 TF families (MYB, NAC, bZIP, bHLH and WRKY) were found for shoot-borne root traits. A total of 19 genes including PIN3, LBD15, IAA32, IAA38 and ARR12 and 19 GWAS signals were overlapped with selective sweeps. Further, significant additive effects were found for root traits, and pyramiding the favorable alleles could enhance maize root development. These findings could contribute to understand the genetic basis of root development and evolution, and provided an important genetic resource for the genetic improvement of root traits in maize.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Arai-Sanoh Y, Takai T, Yoshinaga S, Nakano H, Kojima M, Sakakibara H, Kondo M, Uga Y (2014) Deep rooting conferred by DEEPER ROOTING 1 enhances rice yield in paddy fields. Sci Rep 4:5563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Atwell S, Huang YS, Vilhjalmsson BJ, Willems G, Horton M, Li Y, Meng D, Platt A, Tarone AM, Hu TT, Jiang R, Muliyati NW, Zhang X, Amer MA, Baxter I, Brachi B, Chory J, Dean C, Debieu M, de Meaux J, Ecker JR, Faure N, Kniskern JM, Jones JD, Michael T, Nemri A, Roux F, Salt DE, Tang C, Todesco M, Traw MB, Weigel D, Marjoram P, Borevitz JO, Bergelson J, Nordborg M (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465:627–631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Bellini C, Pacurar DI, Perrone I (2014) Adventitious roots and lateral roots: similarities and differences. Annu Rev Plant Biol 65:639–666

    Article  CAS  PubMed  Google Scholar 

  • Bishopp A, Lynch JP (2015) The hidden half of crop yields. Nat Plants 1:15117

    Article  PubMed  Google Scholar 

  • Brachi B, Morris GP, Borevitz JO (2011) Genome-wide association studies in plants: the missing heritability is in the field. Genome Biol 12:232

    Article  PubMed  PubMed Central  Google Scholar 

  • Buckler ES, Holland JB, Bradbury PJ, Acharya CB, Brown PJ, Browne C, Ersoz E, Flint-Garcia S, Garcia A, Glaubitz JC, Goodman MM, Harjes C, Guill K, Kroon DE, Larsson S, Lepak NK, Li H, Mitchell SE, Pressoir G, Peiffer JA, Rosas MO, Rocheford TR, Romay MC, Romero S, Salvo S, Sanchez Villeda H, da Silva HS, Sun Q, Tian F, Upadyayula N, Ware D, Yates H, Yu J, Zhang Z, Kresovich S, McMullen MD (2009) The genetic architecture of maize flowering time. Science 325:714–718

    Article  CAS  PubMed  Google Scholar 

  • Burton AL, Brown KM, Lynch JP (2013) Phenotypic diversity of root anatomical and architectural traits in zea species. Crop Sci 53:1042–1055

    Article  Google Scholar 

  • Burton AL, Johnson J, Foerster J, Hanlon MT, Kaeppler SM, Lynch JP, Brown KM (2015) QTL mapping and phenotypic variation of root anatomical traits in maize (Zea mays L.). Theor Appl Genet 128:93–106

    Article  PubMed  Google Scholar 

  • Burton AL, Johnson JM, Foerster JM, Hirsch CN, Buell CR, Hanlon MT, Kaeppler SM, Brown KM, Lynch JP (2014) QTL mapping and phenotypic variation for root architectural traits in maize (Zea mays L.). Theor Appl Genet 127:2293–2311

    Article  PubMed  Google Scholar 

  • Cai H, Chen F, Mi G, Zhang F, Maurer HP, Liu W, Reif JC, Yuan L (2012) Mapping QTLs for root system architecture of maize (Zea mays L.) in the field at different developmental stages. Theor Appl Genet 125:1313–1324

    Article  PubMed  Google Scholar 

  • Chimungu JG, Loades KW, Lynch JP (2015) Root anatomical phenes predict root penetration ability and biomechanical properties in maize (Zea Mays). J Exp Bot 66:3151–3162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coudert Y, Le VAT, Adam H, Bes M, Vignols F, Jouannic S, Guiderdoni E, Gantet P (2015) Identification of CROWN ROOTLESS1-regulated genes in rice reveals specific and conserved elements of postembryonic root formation. New Phytol 206:243–254

    Article  CAS  PubMed  Google Scholar 

  • Coudert Y, Perin C, Courtois B, Khong NG, Gantet P (2010) Genetic control of root development in rice, the model cereal. Trends Plant Sci 15:219–226

    Article  CAS  PubMed  Google Scholar 

  • de Dorlodot S, Forster B, Pages L, Price A, Tuberosa R, Draye X (2007) Root system architecture: opportunities and constraints for genetic improvement of crops. Trends Plant Sci 12:474–481

    Article  PubMed  Google Scholar 

  • Den Herder G, Van Isterdael G, Beeckman T, De Smet I (2010) The roots of a new green revolution. Trends Plant Sci 15:600–607

    Article  Google Scholar 

  • Famoso AN, Zhao K, Clark RT, Tung CW, Wright MH, Bustamante C, Kochian LV, McCouch SR (2011) Genetic architecture of aluminum tolerance in rice (Oryza sativa) determined through genome-wide association analysis and QTL mapping. PLoS Genet 7:e1002221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fusi R, Rosignoli S, Lou H, Sangiorgi G, Bovina R, Pattem JK, Borkar AN, Lombardi M, Forestan C, Milner SG, Davis JL, Lale A, Kirschner GK, Swarup R, Tassinari A, Pandey BK, York LM, Atkinson BS, Sturrock CJ, Mooney SJ, Hochholdinger F, Tucker MR, Himmelbach A, Stein N, Mascher M, Nagel KA, De Gara L, Simmonds J, Uauy C, Tuberosa R, Lynch JP, Yakubov GE, Bennett MJ, Bhosale R, Salvi S (2022) Root angle is controlled by EGT1 in cereal crops employing an antigravitropic mechanism. Proc Natl Acad Sci U S A 119:e2201350119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao S, Fang J, Xu F, Wang W, Sun X, Chu J, Cai B, Feng Y, Chu C (2014) CYTOKININ OXIDASE/DEHYDROGENASE4 integrates cytokinin and Auxin signaling to control rice crown root formation. Plant Physiol 165:1035–1046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao Y, Lynch JP (2016) Reduced crown root number improves water acquisition under water deficit stress in maize (Zea mays L.). J Exp Bot 67:4545–4557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gewin V (2010) Food: an underground revolution. Nature 466:552–553

    Article  CAS  PubMed  Google Scholar 

  • Guo H, York LM (2019) Maize with fewer nodal roots allocates mass to more lateral and deep roots that improve nitrogen uptake and shoot growth. J Exp Bot 70:5299–5309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hershko A (2005) The ubiquitin system for protein degradation and some of its roles in the control of the cell division cycle[ast]. Cell Death Differ 12:1191–1197

    Article  CAS  PubMed  Google Scholar 

  • Hochholdinger F, Woll K, Sauer M, Dembinsky D (2004) Genetic dissection of root formation in maize (Zea mays) reveals root-type specific developmental programmes. Ann Bot 93:359–368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hochholdinger F, Yu P, Marcon C (2018) Genetic control of root system development in maize. Trends Plant Sci 23:79–88

    Article  CAS  PubMed  Google Scholar 

  • Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y, Li C, Zhu C, Lu T, Zhang Z, Li M, Fan D, Guo Y, Wang A, Wang L, Deng L, Li W, Lu Y, Weng Q, Liu K, Huang T, Zhou T, Jing Y, Li W, Lin Z, Buckler ES, Qian Q, Zhang QF, Li J, Han B (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42:961–967

    Article  CAS  PubMed  Google Scholar 

  • Hund A, Reimer R, Messmer R (2011) A consensus map of QTLs controlling the root length of maize. Plant Soil 344:143–158

    Article  CAS  Google Scholar 

  • Hung HY, Shannon LM, Tian F, Bradbury PJ, Chen C, Flint-Garcia SA, McMullen MD, Ware D, Buckler ES, Doebley JF, Holland JB (2012) ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize. Proc Natl Acad Sci U S A 109:E1913-1921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Itoh J, Nonomura K, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46:23–47

    Article  CAS  PubMed  Google Scholar 

  • Jeong JS, Kim YS, Redillas MC, Jang G, Jung H, Bang SW, Choi YD, Ha SH, Reuzeau C, Kim JK (2013) OsNAC5 overexpression enlarges root diameter in rice plants leading to enhanced drought tolerance and increased grain yield in the field. Plant Biotechnol J 11:101–114

    Article  CAS  PubMed  Google Scholar 

  • Jia Z, Liu Y, Gruber BD, Neumann K, Kilian B, Graner A, von Wiren N (2019) Genetic dissection of root system architectural traits in spring barley. Front Plant Sci 10:400

    Article  PubMed  PubMed Central  Google Scholar 

  • Jin J, Zhang H, Kong L, Gao G, Luo J (2014) PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res 42:D1182-1187

    Article  CAS  PubMed  Google Scholar 

  • Jung JK, McCouch S (2013) Getting to the roots of it: Genetic and hormonal control of root architecture. Front Plant Sci 4:186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirschner GK, Rosignoli S, Guo L, Vardanega I, Imani J, Altmuller J, Milner SG, Balzano R, Nagel KA, Pflugfelder D, Forestan C, Bovina R, Koller R, Stocker TG, Mascher M, Simmonds J, Uauy C, Schoof H, Tuberosa R, Salvi S, Hochholdinger F (2021) ENHANCED GRAVITROPISM 2 encodes a STERILE ALPHA MOTIF-containing protein that controls root growth angle in barley and wheat. Proc Natl Acad Sci U S A 118:e2101526118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kitomi Y, Hanzawa E, Kuya N, Inoue H, Hara N, Kawai S, Kanno N, Endo M, Sugimoto K, Yamazaki T, Sakamoto S, Sentoku N, Wu J, Kanno H, Mitsuda N, Toriyama K, Sato T, Uga Y (2020) Root angle modifications by the DRO1 homolog improve rice yields in saline paddy fields. Proc Natl Acad Sci U S A 117:21242–21250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kong X, Zhang M, De Smet I, Ding Z (2014) Designer crops: optimal root system architecture for nutrient acquisition. Trends Biotechnol 32:597–598

    Article  CAS  PubMed  Google Scholar 

  • Li H, Peng Z, Yang X, Wang W, Fu J, Wang J, Han Y, Chai Y, Guo T, Yang N, Liu J, Warburton ML, Cheng Y, Hao X, Zhang P, Zhao J, Liu Y, Wang G, Li J, Yan J (2013) Genome-wide association study dissects the genetic architecture of oil biosynthesis in maize kernels. Nat Genet 45:43–50

    Article  CAS  PubMed  Google Scholar 

  • Li MX, Yeung JM, Cherny SS, Sham PC (2012a) Evaluating the effective numbers of independent tests and significant p-value thresholds in commercial genotyping arrays and public imputation reference datasets. Hum Genet 131:747–756

    Article  CAS  PubMed  Google Scholar 

  • Li P, Chen F, Cai H, Liu J, Pan Q, Liu Z, Gu R, Mi G, Zhang F, Yuan L (2015) A genetic relationship between nitrogen use efficiency and seedling root traits in maize as revealed by QTL analysis. J Exp Bot 66:3175–3188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li P, Fan Y, Yin S, Wang Y, Wang H, Xu Y, Yang Z, Xu C (2020) Multi-environment QTL mapping of crown root traits in a maize RIL population. Crop J 8:645–654

    Article  Google Scholar 

  • Li P, Zhang Y, Yin S, Zhu P, Pan T, Xu Y, Wang J, Hao D, Fang H, Xu C, Yang Z (2018) QTL-by-environment interaction in the response of maize root and shoot traits to different water regimes. Front Plant Sci 9:229

    Article  PubMed  PubMed Central  Google Scholar 

  • Li P, Zhuang Z, Cai H, Cheng S, Soomro AA, Liu Z, Gu R, Mi G, Yuan L, Chen F (2016) Use of genotype-environment interactions to elucidate the pattern of maize root plasticity to nitrogen deficiency. J Integr Plant Biol 58:242–253

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Yang X, Xu S, Cai Y, Zhang D, Han Y, Li L, Zhang Z, Gao S, Li J, Yan J (2012b) Genome-wide association studies identified three independent polymorphisms associated with alpha-tocopherol content in maize kernels. PLoS ONE 7:e36807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Wang X, Warburton ML, Wen W, Jin M, Deng M, Liu J, Tong H, Pan Q, Yang X, Yan J (2015) Genomic, transcriptomic, and phenomic variation reveals the complex adaptation of modern maize breeding. Mol Plant 8:871–884

    Article  CAS  PubMed  Google Scholar 

  • Liu HJ, Wang X, Xiao Y, Luo J, Qiao F, Yang W, Zhang R, Meng Y, Sun J, Yan S, Peng Y, Niu L, Jian L, Song W, Yan J, Li C, Zhao Y, Liu Y, Warburton ML, Zhao J, Yan J (2020) CUBIC: an atlas of genetic architecture promises directed maize improvement. Genome Biol 21:20

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Zhao Y, Guo S, Cheng S, Guan Y, Cai H, Mi G, Yuan L, Chen F (2019) Enhanced crown root number and length confers potential for yield improvement and fertilizer reduction in nitrogen-efficient maize cultivars. Field Crops Res 241:107562

    Article  Google Scholar 

  • Lou Q, Chen L, Mei H, Wei H, Feng F, Wang P, Xia H, Li T, Luo L (2015) Quantitative trait locus mapping of deep rooting by linkage and association analysis in rice. J Exp Bot 66:4749–4757

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu Y, Zhang S, Shah T, Xie C, Hao Z, Li X, Farkhari M, Ribaut JM, Cao M, Rong T, Xu Y (2010) Joint linkage-linkage disequilibrium mapping is a powerful approach to detecting quantitative trait loci underlying drought tolerance in maize. Proc Natl Acad Sci U S A 107:19585–19590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynch J (1995) Root architecture and plant productivity. Plant Physiol 109:7–13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynch JP (2013) Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Ann Bot 112:347–357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynch JP, Mooney SJ, Strock CF, Schneider HM (2022) Future roots for future soils. Plant Cell Environ 45:620–636

    Article  CAS  PubMed  Google Scholar 

  • Maqbool S, Hassan MA, Xia X, York LM, Rasheed A, He Z (2022) Root system architecture in cereals: progress, challenges and perspective. Plant J 110:23–42

    Article  CAS  PubMed  Google Scholar 

  • Maurel C, Nacry P (2020) Root architecture and hydraulics converge for acclimation to changing water availability. Nat Plants 6:744–749

    Article  PubMed  Google Scholar 

  • Meng F, Xiang D, Zhu J, Li Y, Mao C (2019) Molecular mechanisms of root development in rice. Rice (n y) 12:1

    Article  PubMed  Google Scholar 

  • Motte H, Vercauteren A, Depuydt S, Landschoot S, Geelen D, Werbrouck S, Goormachtig S, Vuylsteke M, Vereecke D (2014) Combining linkage and association mapping identifies RECEPTOR-LIKE PROTEIN KINASE1 as an essential Arabidopsis shoot regeneration gene. Proc Natl Acad Sci U S A 111:8305–8310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muthreich N, Majer C, Beatty M, Paschold A, Schutzenmeister A, Fu Y, Malik WA, Schnable PS, Piepho HP, Sakai H, Hochholdinger F (2013) Comparative transcriptome profiling of maize coleoptilar nodes during shoot-borne root initiation. Plant Physiol 163:419–430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Omori F, Mano Y (2007) QTL mapping of root angle in F2 populations from maize B73 × teosinte Zea luxurians’. Plant Root 1:57–65

    Article  CAS  Google Scholar 

  • Orman-Ligeza B, Parizot B, Gantet PP, Beeckman T, Bennett MJ, Draye X (2013) Post-embryonic root organogenesis in cereals: branching out from model plants. Trends Plant Sci 18:459–467

    Article  CAS  PubMed  Google Scholar 

  • Pace J, Gardner C, Romay C, Ganapathysubramanian B, Lubberstedt T (2015) Genome-wide association analysis of seedling root development in maize (Zea mays L.). Bmc Genom 16:47

    Article  CAS  Google Scholar 

  • Pace J, Lee N, Naik HS, Ganapathysubramanian B, Lubberstedt T (2014) Analysis of maize (Zea mays L.) seedling roots with the high-throughput image analysis tool ARIA (Automatic Root Image Analysis). PLoS ONE 9:e108255

    Article  PubMed  PubMed Central  Google Scholar 

  • Pan Q, Li L, Yang X, Tong H, Xu S, Li Z, Li W, Muehlbauer GJ, Li J, Yan J (2016) Genome-wide recombination dynamics are associated with phenotypic variation in maize. New Phytol 210:1083–1094

    Article  CAS  PubMed  Google Scholar 

  • Pan Q, Xu Y, Li K, Peng Y, Zhan W, Li W, Li L, Yan J (2017) The genetic basis of plant architecture in 10 maize recombinant inbred line populations. Plant Physiol 175:858–873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38:904–909

    Article  CAS  PubMed  Google Scholar 

  • Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Redillas MC, Jeong JS, Kim YS, Jung H, Bang SW, Choi YD, Ha SH, Reuzeau C, Kim JK (2012) The overexpression of OsNAC9 alters the root architecture of rice plants enhancing drought resistance and grain yield under field conditions. Plant Biotechnol J 10:792–805

    Article  CAS  PubMed  Google Scholar 

  • Rogers ED, Benfey PN (2015) Regulation of plant root system architecture: implications for crop advancement. Curr Opin Biotechnol 32:93–98

    Article  CAS  PubMed  Google Scholar 

  • Ruta N, Liedgens M, Fracheboud Y, Stamp P, Hund A (2010) QTLs for the elongation of axile and lateral roots of maize in response to low water potential. Theor Appl Genet 120:621–631

    Article  CAS  PubMed  Google Scholar 

  • Saengwilai P, Tian X, Lynch JP (2014) Low crown root number enhances nitrogen acquisition from low-nitrogen soils in maize. Plant Physiol 166:581–589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schneider HM, Lor VSN, Hanlon MT, Perkins A, Kaeppler SM, Borkar AN, Bhosale R, Zhang X, Rodriguez J, Bucksch A, Bennett MJ, Brown KM, Lynch JP (2022) Root angle in maize influences nitrogen capture and is regulated by calcineurin B-like protein (CBL)-interacting serine/threonine-protein kinase 15 (ZmCIPK15). Plant Cell Environ 45:837–853

    Article  CAS  PubMed  Google Scholar 

  • Schneider HM, Strock CF, Hanlon MT, Vanhees DJ, Perkins AC, Ajmera IB, Sidhu JS, Mooney SJ, Brown KM, Lynch JP (2021a) Multiseriate cortical sclerenchyma enhance root penetration in compacted soils. Proc Natl Acad Sci 118:e2012087118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schneider HM, Yang JT, Brown KM, Lynch JP (2021) Nodal root diameter and node number in maize (Zea mays L.) interact to influence plant growth under nitrogen stress. Plant Direct 5:e00310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun B, Gao Y, Lynch JP (2018) Large crown root number improves topsoil foraging and phosphorus acquisition. Plant Physiol 177:90–104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939

    Article  CAS  PubMed  Google Scholar 

  • Tian F, Bradbury PJ, Brown PJ, Hung H, Sun Q, Flint-Garcia S, Rocheford TR, McMullen MD, Holland JB, Buckler ES (2011) Genome-wide association study of leaf architecture in the maize nested association mapping population. Nat Genet 43:159–162

    Article  CAS  PubMed  Google Scholar 

  • Trachsel S, Kaeppler SM, Brown KM, Lynch JP (2010) Shovelomics: high throughput phenotyping of maize (Zea mays L.) root architecture in the field. Plant Soil 341:75–87

    Article  Google Scholar 

  • Trachsel S, Kaeppler SM, Brown KM, Lynch JP (2013) Maize root growth angles become steeper under low N conditions. Field Crops Res 140:18–31

    Article  Google Scholar 

  • Tuberosa R, Sanguineti MC, Landi P, Giuliani MM, Salvi S, Conti S (2002) Identification of QTLs for root characteristics in maize grown in hydroponics and analysis of their overlap with QTLs for grain yield in the field at two water regimes. Plant Mol Biol 48:697–712

    Article  CAS  PubMed  Google Scholar 

  • Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N, Kitomi Y, Inukai Y, Ono K, Kanno N, Inoue H, Takehisa H, Motoyama R, Nagamura Y, Wu J, Matsumoto T, Takai T, Okuno K, Yano M (2013) Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat Genet 45:1097–1102

    Article  CAS  PubMed  Google Scholar 

  • van Heerwaarden J, Doebley J, Briggs WH, Glaubitz JC, de GoodmanJesus Sanchez GonzalezRoss-Ibarra MMJJ (2011) Genetic signals of origin, spread, and introgression in a large sample of maize landraces. Proc Natl Acad Sci U S A 108:1088–1092

    Article  PubMed  Google Scholar 

  • Villanueva RAM, Chen ZJ (2019) ggplot2: Elegant Graphics for Data Analysis (2nd ed.). Measurement: Interdisciplinary Research and Perspectives 17:160–167

  • Wang Q, Tian F, Pan Y, Buckler ES, Zhang Z (2014) A SUPER powerful method for genome wide association study. PLoS ONE 9:e107684

    Article  PubMed  PubMed Central  Google Scholar 

  • Wasson AP, Rebetzke GJ, Kirkegaard JA, Christopher J, Richards RA, Watt M (2014) Soil coring at multiple field environments can directly quantify variation in deep root traits to select wheat genotypes for breeding. J Exp Bot 65:6231–6249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao Y, Tong H, Yang X, Xu S, Pan Q, Qiao F, Raihan MS, Luo Y, Liu H, Zhang X, Yang N, Wang X, Deng M, Jin M, Zhao L, Luo X, Zhou Y, Li X, Liu J, Zhan W, Liu N, Wang H, Chen G, Cai Y, Xu G, Wang W, Zheng D, Yan J (2016) Genome-wide dissection of the maize ear genetic architecture using multiple populations. New Phytol 210:1095–1106

    Article  CAS  PubMed  Google Scholar 

  • Xu C, Tai H, Saleem M, Ludwig Y, Majer C, Berendzen KW, Nagel KA, Wojciechowski T, Meeley RB, Taramino G, Hochholdinger F (2015) Cooperative action of the paralogous maize lateral organ boundaries (LOB) domain proteins RTCS and RTCL in shoot-borne root formation. New Phytol 207:1123–1133

    Article  CAS  PubMed  Google Scholar 

  • Yang N, Lu Y, Yang X, Huang J, Zhou Y, Ali F, Wen W, Liu J, Li J, Yan J (2014) Genome wide association studies using a new nonparametric model reveal the genetic architecture of 17 agronomic traits in an enlarged maize association panel. PLoS Genet 10:e1004573

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang X, Gao S, Xu S, Zhang Z, Prasanna BM, Li L, Li J, Yan J (2010) Characterization of a global germplasm collection and its potential utilization for analysis of complex quantitative traits in maize. Mol Breed 28:511–526

    Article  Google Scholar 

  • York LM, Galindo-Castaneda T, Schussler JR, Lynch JP (2015) Evolution of US maize (Zea mays L.) root architectural and anatomical phenes over the past 100 years corresponds to increased tolerance of nitrogen stress. J Exp Bot 66:2347–2358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng Z (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Ersoz E, Lai CQ, Todhunter RJ, Tiwari HK, Gore MA, Bradbury PJ, Yu J, Arnett DK, Ordovas JM, Buckler ES (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42:355–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Zhang X, Lin Z, Wang J, Xu M, Lai J, Yu J, Lin Z (2018) The genetic architecture of nodal root number in maize. Plant J 93:1032–1044

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Li P, Motes CM, Park S, Hirschi KD (2015) CHX14 is a plasma membrane K-efflux transporter that regulates K(+) redistribution in Arabidopsis thaliana. Plant Cell Environ 38:2223–2238

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Hu Y, Dai M, Huang L, Zhou DX (2009) The WUSCHEL-related homeobox gene WOX11 is required to activate shoot-borne crown root development in rice. Plant Cell 21:736–748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng Z, Hey S, Jubery T, Liu H, Yang Y, Coffey L, Miao C, Sigmon B, Schnable JC, Hochholdinger F, Ganapathysubramanian B, Schnable PS (2020) Shared genetic control of root system architecture between Zea mays and sorghum bicolor. Plant Physiol 182:977–991

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Ingram PA, Benfey PN, Elich T (2011) From lab to field, new approaches to phenotyping root system architecture. Curr Opin Plant Biol 14:310–317

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank anonymous reviewers for their critical reading and constructive comments on the manuscript.

Funding

This study was financially supported by the National Key Research and Development Program of China (Grant Nos. 2021YFF1000500 and 2016YFD0100700).

Author information

Authors and Affiliations

  1. State Key Laboratory of Nutrient Use and Management, College of Resources and Environmental Sciences, National Academy of Agriculture Green Development, China Agricultural University, Beijing, 100193, China

    Pengcheng Li, Zhihai Zhang, Gui Xiao, Zheng Zhao, Kunhui He, Qingchun Pan, Guohua Mi, Zhongtao Jia, Fanjun Chen & Lixing Yuan

  2. Jiangsu Key Laboratory of Crop Genetics and Physiology/Co-Innovation Center for Modern Production Technology of Grain Crops, Key Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou, 225009, China

    Pengcheng Li

  3. Key Lab of Plant-Soil Interaction, MOE, Center for Resources, Environment and Food Security, College Resources and Environmental Sciences, China Agricultural University, Beijing, 100193, China

    Qingchun Pan, Guohua Mi, Zhongtao Jia, Fanjun Chen & Lixing Yuan

  4. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China

    Jianbing Yan

  5. National Maize Improvement Center of China, Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University, Beijing, 100193, China

    Xiaohong Yang

  6. Center for Crop Functional Genomics and Molecular Breeding, China Agricultural University, Beijing, 100193, China

    Lixing Yuan

Authors
  1. Pengcheng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhihai Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gui Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zheng Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kunhui He
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiaohong Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Qingchun Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Guohua Mi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Zhongtao Jia
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jianbing Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Fanjun Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Lixing Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Lixing Yuan and Fanjun Chen conceived and designed the study. Pengcheng Li, Zhihai Zhang, Gui Xiao, Zhen Zhao, Kunhui He, Xiaohong Yang and Qingchun Pan conducted experiments. Pengcheng Li, Qingchun Pan and Jianbing Yan analyzed the data. Pengcheng Li, Guohua Mi, Zhongtao Jia, Fanjun Chen and Lixing Yuan wrote the paper. All the authors have read and approved the manuscript.

Corresponding authors

Correspondence to Fanjun Chen or Lixing Yuan.

Ethics declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Yes.

Additional information

Communicated by Lee Hickey.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 13286 kb)

Supplementary file2 (XLSX 572 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, P., Zhang, Z., Xiao, G. et al. Genomic basis determining root system architecture in maize. Theor Appl Genet 137, 102 (2024). https://doi.org/10.1007/s00122-024-04606-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00122-024-04606-z

Search

Navigation