Skip to main content
Log in

Association Analysis of the Maize Gene ZmYS1 with Kernel Mineral Concentrations

  • Original Paper
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

Iron (Fe) is an essential micronutrient for humans, and iron deficiency is the most common micronutrient deficiency worldwide. Research on the genetic basis of iron concentration in maize kernels will provide guidance for the development of iron-rich crops, a major breeding goal to address iron deficiency. The maize Yellow Stripe 1 (ZmYS1) gene encodes a specific transporter that takes up Fe(III)-phytosiderophore complexes into roots. Here, we re-sequenced ZmYS1 gene in 88 elite maize inbred lines and detected the association between the nucleotide polymorphisms and micronutrient concentrations in maize kernels. Our analyses detected a total of 71 sequence variants in ZmYS1, including 61 single nucleotide polymorphisms (SNPs) and 10 insertions and deletions (indels), from the tested population. Fourteen haplotypes, which encode 13 different ZmYS1 proteins, are classified based on the polymorphism in the coding region. Numerous polymorphic sites in maize ZmYS1 locus were found in linkage disequilibrium (LD) that decay with increasing physical distance, and at least 14 recombination events have contributed to the LD and haplotype diversity of this gene. Additionally, our data show that a non-synonymous site in the ZmYS1 gene is associated with the maize kernel Fe concentration, and two other non-synonymous sites with Zinc (Zn) concentration. These findings suggest that the polymorphism in maize ZmYS1 locus may be used for biofortifying kernel mineral concentrations in maize breeding programs.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Andersen JR, Schrag T, Melchinger AE, Zein I, Lubberstedt T (2005) Validation of Dwarf8 polymorphisms associated with flowering time in elite European inbred lines of maize (Zea mays L.). Theoretical and applied genetics (TAG; Theoretische und Angewandte Genetik) 111(2):206–217. doi:10.1007/s00122-005-1996-6

    Article  CAS  Google Scholar 

  • Araki R, Murata J, Murata Y (2011) A novel barley yellow stripe 1-like transporter (HvYSL2) localized to the root endodermis transports metal-phytosiderophore complexes. Plant Cell Physiol 52(11):1931–1940. doi:10.1093/pcp/pcr126

    Article  CAS  PubMed  Google Scholar 

  • Bouis HE, Hotz C, McClafferty B, Meenakshi JV, Pfeiffer WH (2011) Biofortification: a new tool to reduce micronutrient malnutrition. Food Nutr Bull 32(1 Suppl):S31–S40

    PubMed  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23(19):2633–2635. doi:10.1093/bioinformatics/btm308

    Article  CAS  PubMed  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(5941):714–718. doi:10.1126/science.1174276

    Article  CAS  PubMed  Google Scholar 

  • Chakraborti M, Prasanna B, Hossain F, Mazumdar S, Singh AM, Guleria S, Gupta H (2011) Identification of kernel iron-and zinc-rich maize inbreds and analysis of genetic diversity using microsatellite markers. J Plant Biochem Biotechnol 20(2):224–233

    Article  CAS  Google Scholar 

  • Choudhary R, Watson DG (2013) Microwave drying kinetics and quality characteristics of corn. Int J Agric Biol Eng 6(1):90–99

    Google Scholar 

  • Curie C, Briat JF (2003) Iron transport and signaling in plants. Annu Rev Plant Biol 54:183–206. doi:10.1146/annurev.arplant.54.031902.135018

    Article  CAS  PubMed  Google Scholar 

  • Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat JF, Walker EL (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409(6818):346–349. doi:10.1038/35053080

    Article  CAS  PubMed  Google Scholar 

  • Ducrocq S, Madur D, Veyrieras JB, Camus-Kulandaivelu L, Kloiber-Maitz M, Presterl T, Ouzunova M, Manicacci D, Charcosset A (2008) Key impact of Vgt1 on flowering time adaptation in maize: evidence from association mapping and ecogeographical information. Genetics 178(4):2433–2437. doi:10.1534/genetics.107.084830

    Article  PubMed Central  PubMed  Google Scholar 

  • Earl DA (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4(2):359–361

    Article  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164(4):1567–1587

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fan C, Xing Y, Mao H, Lu T, Han B, Xu C, Li X, Zhang Q (2006) GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theoretical and applied genetics (TAG; Theoretische und Angewandte Genetik) 112(6):1164–1171. doi:10.1007/s00122-006-0218-1

    Article  CAS  Google Scholar 

  • Fan C, Yu S, Wang C, Xing Y (2009) A causal C-A mutation in the second exon of GS3 highly associated with rice grain length and validated as a functional marker. Theoretical and applied genetics (TAG; Theoretische und Angewandte Genetik) 118(3):465–472. doi:10.1007/s00122-008-0913-1

    Article  CAS  Google Scholar 

  • Flint-Garcia SA, Thuillet AC, Yu J, Pressoir G, Romero SM, Mitchell SE, Doebley J, Kresovich S, Goodman MM, Buckler ES (2005) Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J Cell Molec Biol 44(6):1054–1064. doi:10.1111/j.1365-313X.2005.02591.x

    Article  CAS  Google Scholar 

  • Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133(3):693–709

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gore MA, Chia JM, Elshire RJ, Sun Q, Ersoz ES, Hurwitz BL, Peiffer JA, McMullen MD, Grills GS, Ross-Ibarra J, Ware DH, Buckler ES (2009) A first-generation haplotype map of maize. Science 326(5956):1115–1117. doi:10.1126/science.1177837

    Article  CAS  PubMed  Google Scholar 

  • Hall D, Tegstrom C, Ingvarsson PK (2010) Using association mapping to dissect the genetic basis of complex traits in plants. Brief Funct Gen 9(2):157–165. doi:10.1093/bfgp/elp048

    Article  CAS  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2(4):618–620

    Article  Google Scholar 

  • Harjes CE, Rocheford TR, Bai L, Brutnell TP, Kandianis CB, Sowinski SG, Stapleton AE, Vallabhaneni R, Williams M, Wurtzel ET, Yan J, Buckler ES (2008) Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification. Science 319(5861):330–333. doi:10.1126/science.1150255

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hudson RR, Kaplan NL (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111(1):147–164

    PubMed Central  CAS  PubMed  Google Scholar 

  • Inoue H, Kobayashi T, Nozoye T, Takahashi M, Kakei Y, Suzuki K, Nakazono M, Nakanishi H, Mori S, Nishizawa NK (2009) Rice OsYSL15 is an iron-regulated iron(III)-deoxymugineic acid transporter expressed in the roots and is essential for iron uptake in early growth of the seedlings. J Biol Chem 284(6):3470–3479. doi:10.1074/jbc.M806042200

    Article  CAS  PubMed  Google Scholar 

  • Jiao Y, Zhao H, Ren L, Song W, Zeng B, Guo J, Wang B, Liu Z, Chen J, Li W, Zhang M, Xie S, Lai J (2012) Genome-wide genetic changes during modern breeding of maize. Nat Genet 44(7):812–815. doi:10.1038/ng.2312

    Article  CAS  PubMed  Google Scholar 

  • Jin T, Zhou J, Chen J, Zhu L, Zhao Y, Huang Y (2013) The genetic architecture of zinc and iron content in maize grains as revealed by QTL mapping and meta-analysis. Breed Sci 63(3):317–324. doi:10.1270/jsbbs.63.317

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kakei Y, Ishimaru Y, Kobayashi T, Yamakawa T, Nakanishi H, Nishizawa NK (2012) OsYSL16 plays a role in the allocation of iron. Plant Mol Biol 79(6):583–594. doi:10.1007/s11103-012-9930-1

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kumar B, Abdel-Ghani AH, Pace J, Reyes-Matamoros J, Hochholdinger F, Lubberstedt T (2014) Association analysis of single nucleotide polymorphisms in candidate genes with root traits in maize (Zea mays L.) seedlings. Plant Sci Int J Experiment Plant Biol 224:9–19. doi:10.1016/j.plantsci.2014.03.019

    CAS  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948. doi:10.1093/bioinformatics/btm404

    Article  CAS  PubMed  Google Scholar 

  • Larsson SJ, Lipka AE, Buckler ES (2013) Lessons from Dwarf8 on the strengths and weaknesses of structured association mapping. PLoS Genet 9(2):e1003246. doi:10.1371/journal.pgen.1003246

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Le Jean M, Schikora A, Mari S, Briat JF, Curie C (2005) A loss-of-function mutation in AtYSL1 reveals its role in iron and nicotianamine seed loading. Plant J Cell Molec Biol 44(5):769–782. doi:10.1111/j.1365-313X.2005.02569.x

    Article  Google Scholar 

  • Lee S, Chiecko JC, Kim SA, Walker EL, Lee Y, Guerinot ML, An G (2009) Disruption of OsYSL15 leads to iron inefficiency in rice plants. Plant Physiol 150(2):786–800. doi:10.1104/pp. 109.135418

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li Q, Li L, Yang X, Warburton ML, Bai G, Dai J, Li J, Yan J (2010a) Relationship, evolutionary fate and function of two maize co-orthologs of rice GW2 associated with kernel size and weight. BMC Plant Biol 10:143. doi:10.1186/1471-2229-10-143

    Article  PubMed Central  PubMed  Google Scholar 

  • Li Q, Yang X, Bai G, Warburton ML, Mahuku G, Gore M, Dai J, Li J, Yan J (2010b) Cloning and characterization of a putative GS3 ortholog involved in maize kernel development. Theoretical and applied genetics (TAG; Theoretische und Angewandte Genetik) 120(4):753–763. doi:10.1007/s00122-009-1196-x

    Article  CAS  Google Scholar 

  • Li X, Zhu C, Yeh CT, Wu W, Takacs EM, Petsch KA, Tian F, Bai G, Buckler ES, Muehlbauer GJ, Timmermans MC, Scanlon MJ, Schnable PS, Yu J (2012) Genic and nongenic contributions to natural variation of quantitative traits in maize. Genome Res 22(12):2436–2444. doi:10.1101/gr.140277.112

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452. doi:10.1093/bioinformatics/btp187

    Article  CAS  PubMed  Google Scholar 

  • Lucca P, Hurrell R, Potrykus I (2002) Fighting iron deficiency anemia with iron-rich rice. J Am Coll Nutr 21(3 Suppl):184S–190S

    Article  CAS  PubMed  Google Scholar 

  • Lung’aho MG, Mwaniki AM, Szalma SJ, Hart JJ, Rutzke MA, Kochian LV, Glahn RP, Hoekenga OA (2011) Genetic and physiological analysis of iron biofortification in maize kernels. PLoS One 6(6):e20429. doi:10.1371/journal.pone.0020429

    Article  PubMed Central  PubMed  Google Scholar 

  • Ma JF (2005) Plant root responses to three abundant soil minerals: silicon, aluminum and iron. Crit Rev Plant Sci 24(4):267–281

    Article  CAS  Google Scholar 

  • Mayer JE, Pfeiffer WH, Beyer P (2008) Biofortified crops to alleviate micronutrient malnutrition. Curr Opin Plant Biol 11(2):166–170. doi:10.1016/j.pbi.2008.01.007

    Article  CAS  PubMed  Google Scholar 

  • Murata Y, Ma JF, Yamaji N, Ueno D, Nomoto K, Iwashita T (2006) A specific transporter for iron(III)-phytosiderophore in barley roots. Plant J Cell Molec Biol 46(4):563–572. doi:10.1111/j.1365-313X.2006.02714.x

    Article  CAS  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8(19):4321–4325

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Prasad AS (2012) Discovery of human zinc deficiency: 50 years later. J Trace Elem Med Biol Org Soc Min Trace Elem 26(2–3):66–69. doi:10.1016/j.jtemb.2012.04.004

    Article  CAS  Google Scholar 

  • Prasanna B, Pixley K, Warburton ML, Xie C-X (2010) Molecular marker-assisted breeding options for maize improvement in Asia. Mol Breed 26(2):339–356

    Article  CAS  Google Scholar 

  • Qin H, Cai Y, Liu Z, Wang G, Wang J, Guo Y, Wang H (2012) Identification of QTL for zinc and iron concentration in maize kernel and cob. Euphytica 187(3):345–358

    Article  CAS  Google Scholar 

  • Rafalski JA (2010) Association genetics in crop improvement. Curr Opin Plant Biol 13(2):174–180. doi:10.1016/j.pbi.2009.12.004

    Article  CAS  PubMed  Google Scholar 

  • Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler ES (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci U S A 98(20):11479–11484. doi:10.1073/pnas.201394398

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Roberts LA, Pierson AJ, Panaviene Z, Walker EL (2004) Yellow stripe1. Expanded roles for the maize iron-phytosiderophore transporter. Plant Physiol 135(1):112–120. doi:10.1104/pp. 103.037572

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Šimić D, Drinić SM, Zdunić Z, Jambrović A, Ledenčan T, Brkić J, Brkić A, Brkić I (2012) Quantitative trait loci for biofortification traits in maize grain. J Hered 103(1):47–54

    Article  PubMed  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585–595

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tako E, Hoekenga OA, Kochian LV, Glahn RP (2013) High bioavailability iron maize (Zea mays L.) developed through molecular breeding provides more absorbable iron in vitro (Caco-2 model) and in vivo (Gallus gallus). Nutr J 12:3. doi:10.1186/1475-2891-12-3

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28(3):286–289. doi:10.1038/90135

    Article  CAS  PubMed  Google Scholar 

  • Ueno D, Yamaji N, Ma JF (2009) Further characterization of ferric-phytosiderophore transporters ZmYS1 and HvYS1 in maize and barley. J Exp Bot 60(12):3513–3520. doi:10.1093/jxb/erp191

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Waters BM, Chu HH, Didonato RJ, Roberts LA, Eisley RB, Lahner B, Salt DE, Walker EL (2006) Mutations in Arabidopsis yellow stripe-like1 and yellow stripe-like3 reveal their roles in metal ion homeostasis and loading of metal ions in seeds. Plant Physiol 141(4):1446–1458. doi:10.1104/pp. 106.082586

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Weng J, Li B, Liu C, Yang X, Wang H, Hao Z, Li M, Zhang D, Ci X, Li X, Zhang S (2013) A non-synonymous SNP within the isopentenyl transferase 2 locus is associated with kernel weight in Chinese maize inbreds (Zea mays L.). BMC Plant Biol 13:98. doi:10.1186/1471-2229-13-98

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wilson LM, Whitt SR, Ibanez AM, Rocheford TR, Goodman MM, Buckler ES (2004) Dissection of maize kernel composition and starch production by candidate gene association. Plant Cell 16(10):2719–2733. doi:10.1105/tpc.104.025700

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xu F, Zhang G, Tong C, Sun X, Corke H, Sun M, Bao J (2013) Association mapping of starch physicochemical properties with starch biosynthesizing genes in waxy rice (Oryza sativa L.). J Agric Food Chem 61(42):10110–10117. doi:10.1021/jf4029688

    Article  CAS  PubMed  Google Scholar 

  • Xue Y, Yue S, Zhang W, Liu D, Cui Z, Chen X, Ye Y, Zou C (2014) Zinc, iron, manganese and copper uptake requirement in response to nitrogen supply and the increased grain yield of summer maize. PLoS One 9(4):e93895. doi:10.1371/journal.pone.0093895

    Article  PubMed Central  PubMed  Google Scholar 

  • Yan J, Kandianis CB, Harjes CE, Bai L, Kim EH, Yang X, Skinner DJ, Fu Z, Mitchell S, Li Q, Fernandez MG, Zaharieva M, Babu R, Fu Y, Palacios N, Li J, Dellapenna D, Brutnell T, Buckler ES, Warburton ML, Rocheford T (2010) Rare genetic variation at Zea mays crtRB1 increases beta-carotene in maize grain. Nat Genet 42(4):322–327. doi:10.1038/ng.551

    Article  CAS  PubMed  Google Scholar 

  • Yan J, Warburton M, Crouch J (2011) Association mapping for enhancing maize (L.) genetic improvement. Crop Sci 51(2):433–449

    Article  Google Scholar 

  • Yang Z, Zhang E, Jiang Y, Xu S, Pan L, Chen Q, Xu C (2014a) Sequence polymorphisms in Zmisa2 gene are significantly associated with starch pasting and gelatinization properties in maize (Zea mays L.). Mol Breed. doi:10.1007/s11032-014-0142-z

    PubMed Central  PubMed  Google Scholar 

  • Yang Z, Zhang E, Li J, Jiang Y, Wang Y, Hu Y, Xu C (2014b) Analyses of sequence polymorphism and haplotype diversity of LEAFY genes revealed post-domestication selection in the Chinese elite maize inbred lines. Mol Biol Rep 41(2):1117–1125. doi:10.1007/s11033-013-2958-8

    Article  PubMed  Google Scholar 

  • Yen MR, Tseng YH, Saier MH Jr (2001) Maize yellow stripe1, an iron-phytosiderophore uptake transporter, is a member of the oligopeptide transporter (OPT) family. Microbiology 147(Pt 11):2881–2883

    Article  CAS  PubMed  Google Scholar 

  • Zhang E, Yang Z, Wang Y, Hu Y, Song X, Xu C (2013) Nucleotide polymorphisms and haplotype diversity of RTCS gene in China elite maize inbred lines. PLoS One 8(2):e56495. doi:10.1371/journal.pone.0056495

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the National Program on the Development of Basic Research (2011CB100100), the Priority Academic Program Development of Jiangsu Higher Education Institutions, the National Natural Science Foundations (31391632, 31200943, and 31171187), the Natural Science Foundations of Jiangsu Province (BK2012261), the Natural Science Foundation of the Jiangsu Higher Education Institutions (14KJA210005), and the Innovative Research Team of Universities in Jiangsu Province.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Chenwu Xu or Jinling Huang.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Supplementary Table 1

The maize inbred lines used in this study. (DOCX 22 kb)

Supplementary Table 2

The nucleotide polymorphisms and their positions in the maize ZmYS1 gene. (XLSX 58 kb)

Supplementary Table 3

Parameters of the nucleotide polymorphisms in 7 exons and 6 introns of the maize ZmYS1 gene. (DOCX 21 kb)

Supplementary Table 4

Distribution of haplotypes of the ZmYS1 gene in 88 inbred lines using both the full-length sequence and coding regions (DOCX 14 kb)

Supplementary Fig. 1

Sequence alignment of maize ZmYS1 proteins encoded by different CDS haplotypes. The haplotypes defined by the coding sequences of the gene ZmYS1 were used as the sequence names. Polymorphisms from inferred amino acids were indicated by boxes. (DOCX 3120 kb)

Supplementary Fig. 2

LD patterns across the whole locus of ZmYS1. (A) LD between pairs of ZmYS1 sequence polymorphic sites. (B) Decay of LD between pairs of ZmYS1 sequence informative polymorphisms. The regression coefficient b is 0.00545. (DOCX 443 kb)

Supplementary Fig. 3

Population structure of 88 maize inbred lines estimated using 3,072 SNPs. (A) Population structure of 88 maize inbred lines when k = 3. (B) Rate of change in the log probability of data between successive k values (Δk). (DOCX 48 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, Z., Ma, S., Hu, Y. et al. Association Analysis of the Maize Gene ZmYS1 with Kernel Mineral Concentrations. Plant Mol Biol Rep 33, 1327–1335 (2015). https://doi.org/10.1007/s11105-014-0836-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-014-0836-8

Keywords

Navigation