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Identification and mapping of two independent recessive loci for the root hairless mutant phenotype in soybean

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Two functional complementation QTLs were identified for root hairless formation in soybean.

Abstract

Root hairs play critical roles not only in nutrient/water uptake from soils, but also in plant–microorganism interactions. However, genetic information about root hair development remains fragmented. We previously identified a soybean natural mutant (RBC-HL) with the root hairless (HL) phenotype. In order to reveal the genetic basis for this phenotype, a polymorphic population was constructed using RBC-HL and a genotype (RBC-NH) with normal root hairs (NH). Three representative phenotypes of root hair formation were observed in the progeny, including NH, medium (MH) and HL. All F1 plants were of the NH type, and the respective segregation ratios in F2, F2:3 and RIL (F5:7) plants fit the theoretical ratio of 15:1, 7:8:1 and 3:1, indicating that the HL mutation is controlled by two independent recessive loci. In order to map HL-associated loci, a high-density genetic map was constructed using 8784 bin markers covering a total genetic distance of 3108.2 cM, and an average distance between adjacent markers of 0.4 cM. Two major QTLs, qRHLa and qRHLb, were identified and mapped on chromosome 01 and 11, and further delimited to interval regions of ~ 289 kb and ~ 1120 kb, respectively. Phylogenetic analysis suggested that the two candidate regions originated from soybean duplication events, where seven pairs of homologous genes shared 86–97% sequence identify. In conclusion, we partially uncovered the genetic mechanism underlying root hair formation in soybean. Namely, two independent recessive loci, qRHLa and qRHLb, containing several candidate genes were predicted to control the root hairless mutant RBC-HL.

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References

  • Abdelhaleem H, Lee GJ, Boerma RH (2011) Identification of QTL for increased fibrous roots in soybean. Theor Appl Genet 122(5):935–946

    Article  Google Scholar 

  • Batenburg FHDV, Jonker R, Kijne JW (2010) Rhizobium induces marked root hair curling by redirection of tip growth: a computer simulation. Plant Physiol 66(3):476–480

    Article  Google Scholar 

  • Bates TR, Lynch JP (2000) Plant growth and phosphorus accumulation of wild type and two root hair mutants of Arabidopsis thaliana (Brassicaceae). Am J Bot 87(7):958–963

    Article  CAS  PubMed  Google Scholar 

  • Bibikova T, Gilroy S (2009) Calcium in root hair growth. In: Emons AM, Ketyelaar T (eds) Plant cell monographs: root hairs. Springer, Berlin, pp 145–170

    Google Scholar 

  • Brown JD (2004) Yates correction factor. Shiken Jalt Test Eval Sig Newsl 8:22–27

    Google Scholar 

  • Cai Z, Cheng Y, Ma Z, Liu X, Ma Q, Xia Q, Zhang G, Mu Y, Nian H (2018) Fine-mapping of QTLs for individual and total isoflavone content in soybean (glycine max l.) using a high-density genetic map. Theor Appl Genet 131(3):555–568

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Liao H (2017) Engineering crop nutrient efficiency for sustainable agriculture. J Integr Plant Biol 59(10):710–735

    Article  PubMed  Google Scholar 

  • Cheng W, Liu F, Li M, Hu X, Chen H, Pappoe F, Luo Q, Wen H, Xing T, Xu Y, Shen J (2015) Variation detection based on next-generation sequencing of type Chinese 1 strains of Toxoplasma gondii with different virulence from China. BMC Genom 16:888

    Article  CAS  Google Scholar 

  • Coale FJ, Meisinger JJ, Wiebold WJ (1985) Effects of plant breeding and selection on yields and nitrogen fixation in soybeans under two soil nitrogen regimes. Plant Soil 86(3):357–367

    Article  Google Scholar 

  • Cristina DM, Sessa G, Dolan L, Linstead P, Baima S, Ruberti I, Morelli G (1996) The Arabidopsis Athb-10 (GLABRA2) is an HD-Zip protein required for regulation of root hair development. Plant J 10(3):393–402

    Article  CAS  PubMed  Google Scholar 

  • Diers BW, Cianzio SR, Shoemaker RC (1992) Possible identification of quantitative trait loci affecting iron efficiency in soybean. J Plant Nutr 15(10):2127–2136

    Article  CAS  Google Scholar 

  • Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujishige NA, Kapadia NN, De Hoff PL, Hirsch AM (2006) Investigations of Rhizobium biofilm formation. FEMS Microbiol Ecol 56(2):195–206

    Article  CAS  PubMed  Google Scholar 

  • Gahoonia TS, Nielsen NE (1998) Direct evidence on participation of root hairs in phosphorus (32P) uptake from soil. Plant Soil 198(2):147–152

    Article  CAS  Google Scholar 

  • Gilroy S, Jones DL (2000) Through form to function: root hair development and nutrient uptake. Trends Plant Sci 5(2):56–60

    Article  CAS  PubMed  Google Scholar 

  • Goormachtig S, Capoen W, Holsters M (2004) Rhizobium infection: lessons from the versatile nodulation behaviour of water-tolerant legumes. Trends Plant Sci 9(11):518–522

    Article  CAS  PubMed  Google Scholar 

  • Grierson CS, Schiefelbein JW (2002) Root hairs. Arabidopsis Book 1:e0060. https://doi.org/10.1199/tab.0060

    Article  PubMed  PubMed Central  Google Scholar 

  • Hanum C (2018) Growth, yield and movement of phosphate nutrients in soybean on P fertilizer, straw mulch and difference of plant spacing. In: IOP conference series: earth and environmental science, vol 122, pp 012051

  • Hatch E, Lazaraton A (1991) The research manual: design and statistics for applied linguistics. Newbury House, Boston

    Google Scholar 

  • Heidarian AR, Kord H, Mostafavi K, Lak AP, Mashhadi FA (2010) Investigating Fe and Zn foliar application on yield and its components of soybean (Glycine max (L) Merr.) at different growth stages. J Agric Biotechnol Sustain Dev 3(9):189–197

    Google Scholar 

  • Hwang S, Ray JD, Cregan PB, King A, Davies MK, Purcell LC (2014) Genetics and mapping of quantitative traits for nodule number, weight, and size in soybean (Glycine max L.[Merr.]). Euphytica 195(3):419–434

    Article  CAS  Google Scholar 

  • Kumudini S, Omielan J, Hume DJ (2008) Soybean genetic improvement in yield and the effect of late-season shading and nitrogen source and supply. Agron J 100(2):278–290

    Article  CAS  Google Scholar 

  • Lan P, Li WF, Lin WD, Santi S, Schmidt W (2013) Mapping gene activity of Arabidopsis root hairs. Genome Biol 14:R67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li D, Lewis RS, Jack AM, Dewey RE, Bowen SW, Miller RD (2012) Development of CAPS and dCAPS markers for CYP82E4, CYP82E5v2 and CYP82E10 gene mutants reducing nicotine to nornicotine conversion in tobacco. Mol Breed 29(3):589–599

    Article  CAS  Google Scholar 

  • Liang Q, Cheng X, Mei M, Yan X, Liao H (2010) QTL analysis of root traits as related to phosphorus efficiency in soybean. Ann Bot 106(1):223–234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin S, Cianzio S, Shoemaker R (1997) Mapping genetic loci for iron deficiency chlorosis in soybean. Mol Breed 3(3):219–229

    Article  CAS  Google Scholar 

  • Liu J, Cai KZ, Luo SM, Zhao CX (2008) Effects of phosphorous treatment on root traits and dry matter accumulation and yield of soybean genotypes with different P efficiency. J Qingdao Agric Univ 25(3):211–214

    CAS  Google Scholar 

  • Liu W, Kim MY, Van K, Lee YH, Li H, Liu X, Lee SH (2011) QTL identification of yield-related traits and their association with flowering and maturity in soybean. J Crop Sci Biotechnol 14(1):65–70

    Article  Google Scholar 

  • Ma Z, Bielenberg DG, Brown KM, Lynch JP (2001) Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant Cell Environ 24(4):459–467

    Article  CAS  Google Scholar 

  • Mace ES, Singh V, Oosterom EJV, Hammer GL, Hunt CH, Jordan DR (2012) QTL for nodal root angle in sorghum (Sorghum bicolor, L. Moench) co-locate with QTL for traits associated with drought adaptation. Theor Appl Genet 124(1):97

    Article  CAS  PubMed  Google Scholar 

  • Masucci JD, Schiefelbein JW (1996) Hormones act downstream of TTG and GL2 to promote root hair outgrowth during epidermis development in the Arabidopsis root. Plant Cell 8(9):1505–1517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mathews A, Carroll BJ, Gresshoff PM (1987) Characterization of non-nodulation mutants of soybean [Glycine max (L.) Merr]: bradyrhizobium effects and absence of root hair curling. J Plant Physiol 131(3):349–361

    Article  Google Scholar 

  • Müller M, Schmidt W (2004) Environmentally induced plasticity of root hair development in Arabidopsis. Plant Physiol 134(1):409–419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neff MM, Turk E, Kalishman M (2002) Web-based primer design for single nucleotide polymorphism analysis. Trends Genet 18(12):613–615

    Article  CAS  PubMed  Google Scholar 

  • Oldroyd GED, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59(1):519–546

    Article  CAS  PubMed  Google Scholar 

  • Orf JH, Chase K, Adler FR, Mansur LM, Lark KG (1999) Genetics of soybean agronomic traits: II. Interactions between yield quantitative trait loci in soybean. Crop Sci 39(6):1652–1657

    Article  Google Scholar 

  • Pitts RJ, Cernac A, Estelle M (2001) Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J 16(5):553–560

    Article  Google Scholar 

  • Qin L, Zhao J, Tian J, Chen L, Sun Z, Guo Y, Lu X, Gu M, Xu G, Liao H (2012) The high-affinity phosphate transporter GmPT5 regulates phosphate transport to nodules and nodulation in soybean. Plant Physiol 159(4):1634–1643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rahman A, Hosokawa S, Oono Y, Amakawa T, Goto N, Tsurumi S (2002) Auxin and ethylene response interactions during Arabidopsis root hair development dissected by auxin influx modulators. Plant Physiol 130(4):1908–1917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ray JD, Dhanapal AP, Singh SK, Valerio HV, Smith JR, Purcell LC, King CA, Boykin D, Cregan PB, Song Q, Fritschi FB (2015) Genome-wide association study of ureide concentration in diverse maturity group IV soybean [Glycine max (L.) Merr.] accessions. G3 Genesgenet 5(11):2391–2403

    Article  CAS  Google Scholar 

  • Rerie WG, Feldmann KA, Marks MD (1994) The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes Dev 8(12):1388–1399

    Article  CAS  PubMed  Google Scholar 

  • Ruijter NCAD, Rook MB, Bisseling T, Emons AMC (1998) Lipochito-oligosaccharides re-initiate root hair tip growth in Vicia sativa with high calcium and spectrin-like antigen at the tip. Plant J 13(3):341–350

    Article  Google Scholar 

  • Sanchez-Contreras M, Bauer WD, Gao M, Robinson JB, Downie JA (2007) Quorum-sensing regulation in rhizobia and its role in symbiotic interactions with legumes. Philos Trans R Soc Lond 362(1483):1149–1163

    Article  CAS  Google Scholar 

  • Schellmann S, Hulskamp M, Uhrig J (2007) Epidermal pattern formation in the root and shoot of Arabidopsis. Biochem Soc Trans 35(Pt1):146–148

    Article  CAS  PubMed  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W (2010) Genome sequence of the palaeopolyploid soybean. Nature 463(7278):178–183

    Article  CAS  PubMed  Google Scholar 

  • Shaw SH, Long SR (2003) Nod factor elicits two separable calcium responses in Medicago truncatula root hair cells. Plant Physiol 131(3):976–984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stetter MG, Schmid K, Ludewig U (2015) Uncovering genes and ploidy involved in the high diversity in root hair density, length and response to local scarce phosphate in Arabidopsis thaliana. PLoS ONE 10(3):e0120604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Todd CD, Polacco JC (2004) Soybean cultivars ‘Williams 82’ and ‘Maple Arrow’ produce both urea and ammonia during ureide degradation. J Exp Bot 55(398):867–877

    Article  CAS  PubMed  Google Scholar 

  • Tominaga-wada R, Ishida T, Wada T (2011) New insights into the mechanism of development of Arabidopsis root hairs and trichomes. Int Rev Cell Mol Biol 286:67–106

    Article  CAS  PubMed  Google Scholar 

  • Turgeon BG, Bauer WD (1982) Early events in the infection of soybean by Rhizobium japonicum. Time course and cytology of the initial infection process. Can J Bot 60(2):152–161

    Article  Google Scholar 

  • Van Ooijen JW (2004) MapQTL®5. Software for the mapping of quantitative trait loci in experimental populations. Wageningen, Kyazma B V

    Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78

    Article  CAS  PubMed  Google Scholar 

  • Wais RJ, Keating DH, Long SR (2014) Structure-function analysis of nod factor-induced root hair calcium spiking in rhizobium-legume symbiosis. Plant Physiol 129(1):211–224

    Article  CAS  Google Scholar 

  • Wang XR, Yan XL, Liao H (2010) Genetic improvement for phosphorus efficiency in soybean: a radical approach. Ann Bot 106(1):215–222

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang G, Sheng L, Zhao D, Sheng J, Wang X, Liao H (2016) Allocation of nitrogen and carbon is regulated by nodulation and mycorrhizal networks in soybean/maize intercropping system. Front Plant Sci 7:1901

    PubMed  PubMed Central  Google Scholar 

  • Waters BM, Blevins DG (2000) Ethylene production, cluster root formation, and localization of iron (III) reducing capacity in Fe deficient squash roots. Plant Soil 225(1–2):21–31

    Article  CAS  Google Scholar 

  • Xia Z, Zhai H, Liu B, Kong F, Yuan X, Wu H, Cober ER, Harada K (2012) Molecular identification of genes controlling flowering time, maturity, and photoperiod response in soybean. Plant Syst Evol 298(7):1217–1227

    Article  CAS  Google Scholar 

  • Xing S, Li X, Zhang X, Yang Y (1998) Effects of calcium on growth and development of seed root and root hair in wheat. Chin Bull Bot 15(2):41–45

    Google Scholar 

  • Yan XL, Liao H, Beebe SE, Blair MW, Lynch JP (2004) QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant Soil 265(1–2):17–29

    Article  CAS  Google Scholar 

  • Yang Y, Zhao Q, Li X, Liu D, Qi W, Zhang M, Yang C, Liao H (2017) Characterization of genetic basis on synergistic interactions between root architecture and biological nitrogen fixation in soybean. Front Plant Sci 8:1466

    Article  PubMed  PubMed Central  Google Scholar 

  • Yao ZF, Liang CY, Zhang Q, Chen ZJ, Xiao BX, Tian J, Liao H (2014) SPX1 is an important component in the phosphorus signalling network of common bean regulating root growth and phosphorus homeostasis. J Exp Bot 65(12):3299–3310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin X, Bellaloui N, McClure AM, Tyler DD, Mengistu A (2016) Phosphorus fertilization differentially influences fatty acids, protein, and oil in soybean. Am J Plant Sci 7(14):1975–1992

    Article  CAS  Google Scholar 

  • Zanatta TS, Manica-Berto R, Ferreira CD, Cardozo MM, Zambiazi RC, Dias ARG (2016) Phosphate fertilizer and growing environment change the phytochemicals, oil quality, and nutritional composition of roundup ready genetically modified and conventional soybean. J Agric Food Chem 65(13):2661

    Article  CAS  Google Scholar 

  • Zhang X, Zhai H, Wang Y, Tian X, Zhang Y, Wu H, Lü S, Yang G, Li Y, Wang L, Hu B, Bu Q, Xia Z (2016) Functional conservation and diversification of the soybean maturity gene E1 and its homologs in legumes. Sci Rep 6:29548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang DJ, Yang YJ, Liu CY, Zhang F, Hu W, Gong SB, Wu QS (2018) Auxin modulates root-hair growth through its signaling pathway in citrus. Sci Hortic Amsterdam 236:73–78

    Article  CAS  Google Scholar 

  • Zhou Z, Zhang C, Zhou Y, Hao Z, Wang Z, Zeng X, Di H, Li M, Zhang D, Yong H, Zhang S, Weng J, Li X (2016) Genetic dissection of maize plant architecture with an ultra-high density bin map based on recombinant inbred lines. BMC Genom 17(1):178

    Article  CAS  Google Scholar 

  • Zhu J, Kaeppler SM, Lynch JP (2005) Mapping of QTL controlling root hair length in maize (Zea mays L.) under phosphorus deficiency. Plant Soil 270(1):299–310

    Article  CAS  Google Scholar 

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Acknowledgements

We would like to acknowledge Dr. Thomas Walk at North Dakota State University for critical reading. The work is supported by the Ministry of Science and Technology Key Research and Development program (2016YFD0100700) to HL, and we also would like to thanks K + S Group for providing scholarship to HLv.

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  1. Yongqing Yang and Huiyong Lv have contributed equally to this work.

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  1. Root Biology Center, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, 350002, China

    Yongqing Yang, Huiyong Lv & Hong Liao

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  1. Yongqing Yang
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Correspondence to Hong Liao.

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Communicated by Istvan Rajcan.

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Yang, Y., Lv, H. & Liao, H. Identification and mapping of two independent recessive loci for the root hairless mutant phenotype in soybean. Theor Appl Genet 132, 301–312 (2019). https://doi.org/10.1007/s00122-018-3217-0

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