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Heterotic loci analysis for root traits of maize seedlings using an SSSL test population under different nitrogen conditions

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Abstract

Exploitation of heterosis is an efficient strategy to increase crop production, improve quality, and enhance resistance to biotic and abiotic stresses. However, heterosis shows significant genetic × environment effects. Nitrogen is an important nutrient that affects crop development and grain yield. Hybrid maize performs significantly and differently depending on the nitrogen conditions, but the genetic basis of maize heterosis under different nitrogen conditions is unclear. In this study, a test population comprising a set of single segment substitution lines (SSSLs) was used to identify heterotic loci (HL) for root-related traits of maize seedlings under two nitrogen conditions. We identified 80 HL for the root system and related traits in maize seedlings, consisting of 16, 18, 10, 11, 11, and 14 HL associated with root length (RL), root surface area (RSA), root average diameter (RAD), shoot dry weight (SDW), root dry weight (RDW), and plant height (PH), respectively. Among them, 13% of the HL were detected under both nitrogen conditions simultaneously, including the HLs hRL1b, hRL7, hRL9, hRSA7a, hRSA9a, hRAD1a, hSDW6, hSDW7a, hSDW7b, and hPH6a, but most of the HLs (87%) were not detected under both nitrogen conditions. The results indicated that, in maize, heterosis also exists in the interaction between genotype and nitrogen level.

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References

  • Astrid H, Andreas M, Klaus P (2012) Detection of nitrogen deficiency QTL in juvenile wild barley introgression lines growing in a hydroponic system. BMC Genetics 13:88

  • Bi YM, Meyer A, Downs GS, Shi X, El-Kereamy A, Lukens L, Rothstein SJ (2014) High throughput RNA sequencing of a hybrid maize and its parents shows different mechanisms responsive to nitrogen limitation. BMC Genomics 15:77

  • Chun L, Chen FJ, Zhang FS, Mi GH (2005) Root growth, nitrogen uptake and yield formation of hybrid maize with different N efficiency. Plant Nutr. Fertilizer Sci 11:615–619

    Google Scholar 

  • Cregan RF, Mangan BJ, Knight JC, Birks TA, Russell PS, Roberts PJ, Allan DC (1999) Single-mode photonic band gap guidance of light in air. Science 285:1537–1539

    Article  CAS  PubMed  Google Scholar 

  • Ekanayake IJ, O'toole JC, Garrity DP, Masajo TM (1985) Inheritance of root characters and their relations to drought resistance in rice. Crop Sci 25:927–933

    Article  Google Scholar 

  • Erisman JW, Vries W (2000) Nitrogen deposition and effects in European forests. Environ Rev 8:65–93

    Article  CAS  Google Scholar 

  • Feng Y, Cao LY, Wu WM, Shen XH, Zhan XD, Zhai RR, Wang R, Chen DB, Cheng SH (2010) Mapping QTLs for nitrogen-deficiency tolerance at seedling stage in rice (Oryza sativa L.). Plant Breed 129:652–656

    Article  CAS  Google Scholar 

  • Frascaroli E, Canè MA, Landi P, Pea G, Gianfranceschi L, Villa M, Morgante M, Pè ME (2007) Classical genetic and quantitative trait loci analyses of heterosis in a maize hybrid between two elite inbred lines. Genetics 176:625–644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frink CR, Waggoner PE, Ausubel JH (1999) Nitrogen fertilizer: retrospect and prospect. Proc Natl Acad Sci U S A 96:1175–1180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gelli M, Konda AR, Liu K, Zhang C, Clemente TE, Holding DR,  Dweikat IM (2017) Validation of QTL mapping and transcriptome profiling for identification of candidate genes associated with nitrogen stress tolerance in sorghum. BMC Plant Biol 17:123

  • Good AG, Beatty PH (2011) Fertilizing nature: a tragedy of excess in the commons. PLoS Biol 9:e1001124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo X, Guo YP, Ma J, Wang F, Sun MZ, Gui LJ, Zhou JJ, Song XL, Sun XZ, Zhang TZ (2013) Mapping heterotic loci for yield and agronomic traits using chromosome segment introgression lines in cotton. J Integr Plant Biol 55:759–774

    Article  CAS  PubMed  Google Scholar 

  • Guo T, Yang N, Tong H, Pan Q, Yang X, Tang J, Wang J, Li J, Yan J (2014) Genetic basis of grain yield heterosis in an “immortalized F2” maize population. Theor Appl Genet 127:2149–2158

    Article  PubMed  Google Scholar 

  • Guo Z, Lv P, Zhang X, Sun G, Wang H, Li W, Fu Z, Tang J (2016) Identification of heterotic loci for kernel related traits using a maize introgression lines test population. Sci Agric Sin 49:621–631

    CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1937) The water-culture method for growing plants without soil. Calif Agric Exp Stn Circ 347:357–359

    Google Scholar 

  • Hua JP, Xing YZ, Wu WR, Xu CG, Sun XL, Yu SB, Zhang QF (2003) Single-locus heterotic effects and dominance by dominance interactions can adequately explain the genetic basis of heterosis in an elite rice hybrid. Proc Natl Acad Sci U S A 100:2574–2579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang K, Liberatore KL, Park SJ, Alvarez JP, Lippman ZB (2013) Tomato yield heterosis is triggered by a dosage sensitivity of the florigen pathway that fine-tunes shoot architecture. PLoS Genet 9:e1004043

    Article  PubMed  PubMed Central  Google Scholar 

  • Lawrence LR, Ketterings QM, Cherney JH (2008) Effect of nitrogen application on yield and quality of silage corn after forage legume-grass. Agron J 100:73–79

    Article  CAS  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

  • Li Q, Wu YW, Chen W, Jin R, Kong FL, Ke YP, Shi HC, Yuan JC (2017) Cultivar differences in root nitrogen uptake ability of maize hybrids. Front Plant Sci 8:1060

    Article  PubMed  PubMed Central  Google Scholar 

  • Lian X, Xing Y, Yan H, Xu C, Li X, Zhang Q (2005) QTLs for low nitrogen tolerance at seedling stage identified using a recombinant inbred line population derived from an elite rice hybrid. Theor Appl Genet 112:85–96

    Article  CAS  PubMed  Google Scholar 

  • Liu JC, Li JS, Chen FJ, Zhang FS, Ren TH, Zhuang ZJ, Mi GH (2008) Mapping QTLs for root traits under different nitrate levels at the seedling stage in maize (Zea mays L). Plant Soil 305:253–265

    Article  CAS  Google Scholar 

  • Liu GF, Zhu HT, Zhang GQ, Li LH, Ye GY (2012) Dynamic analysis of QTLs on tiller number in rice (Oryza sativa L.) with single segment substitution lines. Theor Appl Genet 125:143–153

    Article  PubMed  Google Scholar 

  • Liu X, Ying Z, Han W, Tang A, Shen J, Cui Z, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang F (2013) Enhanced nitrogen deposition over China. Nature 494:459

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Wang Q, Chen M, Ding Y, Yang X, Liu J, Li X, Zhou C et al (2019) Genome-wide identification and analysis of heterotic loci in three maize hybrids. Plant Biotechnol J. https://doi.org/10.1111/pbi.13186

  • Lu H, Romero-Severson J, Bernarbo R (2003) Genetic basis of heterosis explored by simple sequence repeat markers in a random-mated maize population. Theor Appl Genet 107:494–502

    Article  CAS  PubMed  Google Scholar 

  • Messmer R, Fracheboud Y, Bänziger M, Mateo V, Peter S, Ribaut JM (2009) Drought stress and tropical maize: QTL-by-environment interactions and stability of QTLs across environments for yield components and secondary traits. Theor Appl Genet 119:913–930

    Article  PubMed  Google Scholar 

  • Meyer RC, Kusterer B, Lisec J, Steinfath M, Becher M, Scharr H, Melchinger AE, Selbig J, Schurr U, Willmitzer L, Altmann T (2010) QTL analysis of early stage heterosis for biomass in Arabidopsis. Theor Appl Genet 120:227–237

    Article  PubMed  Google Scholar 

  • Miller AJ, Cramer MD (2004) Root nitrogen acquisition and assimilation. Plant Soil 274:1–36

    Article  CAS  Google Scholar 

  • Paschold A, Jia Y, Marcon C, Lund S, Larson NB, Yeh CT, Ossowski S, Lanz C, Nettleton D, Schnable PS, Hochholdinger F (2012) Complementation contributes to transcriptome complexity in maize (Zea mays L.) hybrids relative to their inbred parents. Genome Res 22:2445–2454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reif JC, Zhao Y, Würschum T, Gowda M, Hahn V (2013) Genomic prediction of sunflower hybrid performance. Plant Breed 132:107–114

    Article  CAS  Google Scholar 

  • Ribaut JB, Fracheboud Y, Monneveux P, Banziger M, Vargas M, Jiang CJ (2007) Quantitative trait loci for yield and correlated traits under high and low nitrogen conditions in tropical maize. Mol Breed 20:15–29

    Article  CAS  Google Scholar 

  • Rockenbach MF, Corrêa CCG, Heringer AS, Freitas ILJ, Santa-Catarina SC, Amaral-Júnior AT, Silveira V (2018) Differentially abundant proteins associated with heterosis in the primary roots of popcorn. PLoS One 13:e0197114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Semel Y, Nissenbaum J, Menda N, Zinder M, Krieger U, Issman N, Pleban T, Lippman Z, Gur A, Zamir D (2006) Overdominant quantitative trait locus for yield and fitness in tomato. Proc Natl Acad Sci U S A 103:12981–12986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shang LG, Cai SH, Ma LL, Wang YM, Abduweli A, Wang MY, Wang XC, Liang QZ, Hua JP (2016) Seedling root QTLs analysis on dynamic development and upon nitrogen deficiency stress in upland cotton. Euphytica 207:645–663

    Article  CAS  Google Scholar 

  • Sharma S, Xu S, Ehdaie B, Hoops A, Close TJ, Lukaszewski AJ, Waines JG (2011) Dissection of QTL effects for root traits using a chromosome arm-specific mapping population in bread wheat. Theor Appl Genet 122:759–769

    Article  PubMed  Google Scholar 

  • Shen GJ, Zhan W, Chen HX, Xing YZ (2014) Dominance and epistasis are the main contributors to heterosis for plant height in rice. Plant Sci 215:11–18

    Article  CAS  PubMed  Google Scholar 

  • Shull GH (1908) The composition of a field of maize. Am Breed Assn 4:296–301

    Google Scholar 

  • Tang JH, Yan JB, Ma XQ, Teng WT, Wu WR, Dai JR, Dhillon BS, Melchinger AE, Li JS (2010) Dissection of the genetic basis of heterosis in an elite maize hybrid by QTL mapping in an immortalized F2 population. Theor Appl Genet 120:333–340

    Article  PubMed  Google Scholar 

  • Tuberosa R, Sanguineti MC, Landi P, Giuliani MM, Salvi S, Conti S (2002) Identification of QTLs for root characteristics in maize 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 

  • Veldboom LR, Lee M (1996) Genetic mapping of quantitative trait loci in maize in stress and nonstress environments: I. grain yield and yield components. Crop Sci 36:1310–1319

    Article  CAS  Google Scholar 

  • Wang Y, Mi G, Chen F, Zhang J, Zhang F (2004) Response of root morphology to nitrate supply and its contribution to nitrogen accumulation in maize. Plant Nutr 27:2189–2202

    Article  CAS  Google Scholar 

  • Wang ZQ, Yu CY, Xi L, Liu SJ, Yin CB, Liu LL, Lei JG, Jiang L, Yang C, Chen LM, Zhai HQ, Wan JM (2012) Identification of Indica rice chromosome segments for the improvement of japonica inbreds and hybrids. Theor Appl Genet 124:1351–1364

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Zhang X, Yang H, Liu X, Li H, Yuan L, Li W, Fu Z, Tang J, Kang D (2016) Identification of heterotic loci associated with grain yield and its components using two CSSL test populations in maize. Sci Rep 6:38205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei X, Wang B, Peng Q, Wei F, Mao K, Zhang X, Sun P, Liu Z, Tang J (2015) Heterotic loci for various morphological traits of maize detected using a single segment substitution lines test-cross population. Mol Breed 35:1–13

    Article  CAS  Google Scholar 

  • Worku M, Bänziger M, Erley GSA, Friesen D, Diallo AO, Horst WJ (2007) Nitrogen uptake and utilization in contrasting nitrogen efficient tropical maize hybrids. Crop Sci 47:519–528

    Article  CAS  Google Scholar 

  • Wu Q, Chen F, Chen Y, Yuan L, Zhang F, Mi G (2011) Root growth in response to nitrogen supply in Chinese maize hybrids released between 1973 and 2009. Sci China Life Sci 54:642–650

    Article  PubMed  Google Scholar 

  • Xing Z, Tan F, Hua P, Sun L, Zhang QF (2002) Characterization of the main effects, epistatic effects and their environmental interactions of QTLs on the genetic basis of yield traits in rice. Theor Appl Genet 105:248–257

    Article  CAS  PubMed  Google Scholar 

  • Yang H, Lin Y, Zhang HS, Wei XY, Ding D, Xue YD (2017) Mapping of QTLs and heterotic loci for flowering time-related traits in maize. Acta Agron Sin 43:678–690

  • Yi Q, Liu Y, Hou X, Zhang X, Li H, Zhang J, Liu H, Hu Y, Yu G, Li Y, Wang Y, Huang Y (2019) Genetic dissection of yield-related traits and mid-parent heterosis for those traits in maize (Zea mays L.). BMC Plant Biol 19:392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Xue YG, Wang ZQ, Yang JC, Zhang JH (2009) Morphological and physiological traits of roots and their relationships with shoot growth in “super” rice. Field Crops Res 113:31–40

    Article  CAS  Google Scholar 

  • Zhang J, Li G, Li H, Pu X, Jiang J, Chai L, Zheng B, Cui C, Yang Z, Zhu Y, Jiang L (2015) Transcriptome analysis of interspecific hybrid between Brassica napus and B. rapa reveals heterosis for oil rape improvement. Int J Genomics 2015:230985

    PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We also thank Jennifer Smith, PhD, from Liwen Bianji, Edanz Group China (www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript.

Funding

This research was supported by the National Key Research and Development Program of China (2016YFD0101003), the National Natural Science Foundation of China (U1404317), and the Key Grant Science and Technique Foundation of Henan Province (161100110500-0102).

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Author notes

  1. Mengmeng Xu and Xiaomin Lu contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Wheat and Maize Crops Science, College of Agronomy, Henan Agricultural University, Zhengzhou, China

    Mengmeng Xu, Xiaomin Lu, Xiaojing Sun, Huili Yang, Pengshuai Yan, Xiaoyang Chen & Jihua Tang

  2. Henan Academy of Agricultural Sciences, Zhengzhou, China

    Xiaomin Lu

  3. Hubei Collaborative Innovation Center for Grain Industry, Yangtze University, Jingzhou, China

    Hewei Du & Jihua Tang

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  1. Mengmeng Xu
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Contributions

The study was conceived by JT and XC. The data were collected and analyzed by MX, XL, XS, HY, PY, and HD. MX and XL wrote the manuscript. All authors read and approved the final manuscript.

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Correspondence to Xiaoyang Chen or Jihua Tang.

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Xu, M., Lu, X., Sun, X. et al. Heterotic loci analysis for root traits of maize seedlings using an SSSL test population under different nitrogen conditions. Mol Breeding 40, 34 (2020). https://doi.org/10.1007/s11032-020-1110-4

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