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Fine-mapping QTLs and the validation of candidate genes for Aluminum tolerance using a high-density genetic map

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Abstract

Aims

Aluminium (Al) stress is one of the most adverse abiotic factors limiting the growth and productivity of crops in acidic soils. Fine-mapping and cloning of quantitative trait loci (QTLs) provides an effective tool in analysing the genetic mechanisms underlying Al tolerance and in breeding Al-tolerant soybean varieties.

Methods

Soybean cultivar Huachun2 in South China has been reported to be highly tolerant to multiple abiotic stresses in acidic soils, including Al stress. Here, we employ a recombinant inbred line (RIL) population derived from a cross of Huachun2 and Wayao to investigate the Al-tolerance QTLs. The prioritization method and qRT-PCR were applied to predict candidate genes in each QTL. Additionally, the functions of GmGSTU9 and GmPrx145 were investigated in transgenic soybean hairy roots.

Results

In total, five QTLs associated with relative root elongation and Al content were identified by using the high-density genetic map in hydroponics. GmGSTU9, which encodes a glutathione S-transferase gene in qAl06, and GmPrx145, which encodes a class III peroxidase gene in qAl-HC2, were selected to further study the gene functions by using transgenic soybean hairy roots. In transgenic soybean hairy roots, the MDA, H2O2 and O2 contents in GmGSTU9- and GmPrx145-overexpressing hairy roots were lower than those in the control and RNA-interference-exposed hairy roots under Al stress.

Conclusions

GmGSTU9 and GmPrx145 detected in qAl06 and qAl-HC2, respectively, positively regulate Al tolerance in soybean hairy roots by improving the antioxidant activity. These Al tolerance genes and molecular markers will be useful for marker-assisted selection to improve the Al tolerance of soybeans in acidic soils.

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Data availability

The data sets supporting the results of this study are included in the manuscript. Soybean seeds are available from the Guangdong Subcenter of the National Center for Soybean Improvement, PR China.

Abbreviations

CIM:

composite interval mapping method

ICP-AES:

Inductively coupled plasma-atomic emission spectrometry

GST:

glutathione S-transferase

LOD:

log-likelihood

MAS:

marker-assisted selection

NCBI:

National Center for Biotechnology Information

qRT-PCR:

real-time quantitative polymerase chain reaction

QTL:

quantitative trait loci

RAD-seq:

restriction-site associated DNA sequencing

RIL:

Recombinant inbred line

RT-PCR:

reverse transcription-polymerase chain reaction

SNP:

single nucleotide polymorphism

References

  • Abdel-Haleem H, Carter TE, Rufty TW et al (2014) Quantitative trait loci controlling aluminum tolerance in soybean: candidate gene and single nucleotide polymorphism marker discovery. Mol Breed 33(4):851–862

    CAS  Google Scholar 

  • Alam SM (1981) Influence of aluminium on plant growth and mineral nutrition of barley. Commun Soil Sci Plant Anal 12(2):121–138

    CAS  Google Scholar 

  • Amenós M, Corrales I, Poschenrieder C et al (2009) Different effects of aluminum on the actin cytoskeleton and brefeldin A-sensitive vesicle recycling in root apex cells of two maize varieties differing in root elongation rate and aluminum tolerance. Plant Cell Physiol 50(3):528–540

    PubMed  Google Scholar 

  • Bai L, Liu Y, Mu Y et al (2018) Heterotrimeric G-protein γ subunit CsGG3. 2 positively regulates the expression of CBF genes and chilling tolerance in cucumber. Front Plant Sci 9:488

    PubMed  PubMed Central  Google Scholar 

  • Balakumar T, Sivaguru M, James MR et al (1992) Impact of aluminium toxicity on growth and efficiency of nutrient metabolism in some tropical rice cultivars. Trop Agric (Trinidad) 69:211–216

    CAS  Google Scholar 

  • Bargsten JW, Nap JP, Sanchez-Perez GF et al (2014) Prioritization of candidate genes in QTL regions based on associations between traits and biological processes. BMC Plant Biol 14(1):330

    PubMed  PubMed Central  Google Scholar 

  • Bela K, Horváth E, Gallé Á et al (2015) Plant glutathione peroxidases: emerging role of the antioxidant enzymes in plant development and stress responses. J Plant Physiol 176:192–201

    CAS  PubMed  Google Scholar 

  • Bianchi-Hall CM, Carter TE, Ruffy TW et al (1998) Heritability and resource allocation of aluminum tolerance derived from soybean PI 416937. Crop Sci 38(2):513–522

    CAS  Google Scholar 

  • Bianchi-Hall CM, Carter TE, Bailey MA et al (2000) Aluminum tolerance associated with quantitative trait loci derived from soybean PI 416937 in hydroponics. Crop Sci 40(2):538–545

    CAS  Google Scholar 

  • Cai Z, Cheng Y, Xian P et al (2018) Acid phosphatase gene GmHAD1 linked to low phosphorus tolerance in soybean, through fine mapping. Theor Appl Genet 131(8):1715–1728

    CAS  PubMed  Google Scholar 

  • Castrejón SE, Yatsimirsky AK (1997) Cyclodextrin enhanced fluorimetric determination of malonaldehyde by the thiobarbituric acid method. Talanta 44(6):951–957

    PubMed  Google Scholar 

  • Chen L, Cai Y, Liu X et al (2018) GmGRP-like gene confers Al tolerance in Arabidopsis. Sci Rep 8(1):13601

    PubMed  PubMed Central  Google Scholar 

  • Cheng F, Cao G, Wang X et al (2008) The discovery and application of the efficient strains of soybean rhizobia in the acid low phosphorus soil in South China. Chin Sci Bull 23:2903–2910

    Google Scholar 

  • Cheng Y, Ma Q, Ren H et al (2017) Fine mapping of a Phytophthora-resistance gene RpsWY in soybean (Glycine max L.) by high-throughput genome-wide sequencing. Theor Appl Genet 130(5):1041–1051

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ding ZJ, Yan JY, Xu XY et al (2013) WRKY 46 functions as a transcriptional repressor of ALMT 1, regulating aluminum-induced malate secretion in Arabidopsis. Plant J 76(5):825–835

    CAS  PubMed  Google Scholar 

  • Ding C, Chen T, Yang Y et al (2015) Molecular cloning and characterization of an S-adenosylmethionine synthetase gene from Chorispora bungeana. Gene 572(2):205–213

    CAS  PubMed  Google Scholar 

  • Dong D, Thornton I, Ramsey MH (1993) Influence of soil-extractable aluminium and pH on the uptake of aluminium from soil into the soybean plant (Glycine max). Environ Geochem Health 15(2–3):105–111

    CAS  PubMed  Google Scholar 

  • Eggert E, Obata T, Gerstenberger A et al (2016) A sucrose transporter-interacting protein disulphide isomerase affects redox homeostasis and links sucrose partitioning with abiotic stress tolerance. Plant Cell Environ 39(6):1366–1380

    CAS  PubMed  Google Scholar 

  • Ezaki B, Suzuki M, Motoda H et al (2004) Mechanism of gene expression of Arabidopsis glutathione S-transferase, AtGST1, and AtGST11 in response to aluminum stress. Plant Physiol 134(4):1672–1682

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fageria NK, Wright RJ, Ballgar VC (1988) Rice cultivar response to aluminum in nutrient solution. Commun Soil Sci Plant Anal 19(7–12):1133–1142

    CAS  Google Scholar 

  • Foy CD (1984) Physiological Effects of Hydrogen, Aluminum, and Manganese Toxicities in Acid Soil 1. Soil acidity and liming, (soilacidityandl): 57–97

  • Garcia O, Dasilva WJ, Massei MAS. (1979) Efficient method for screening maize inbreds for aluminum tolerance. Maydica

  • Gratão PL, Polle A, Lea PJ et al (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32(6):481–494

    Google Scholar 

  • Grimme H. (1984) Aluminium tolerance of soybean plants as related to magnesium nutrition[C]//6. Colloque international pour l'optimisation de la nutrition des plantes, Montpellier (France), 2-8 Sep 1984. GERDAT

  • Gudys K, Guzy-Wrobelska J, Janiak A, et al. (2018) Prioritization of candidate genes in qtl regions for physiological and biochemical traits underlying drought response in barley (Hordeum vulgare L.). Frontiers in plant science, 9

  • Harper JE (1974) Soil and symbiotic nitrogen requirements for optimum soybean production 1. Crop Sci 14(2):255–260

    CAS  Google Scholar 

  • Hiraga S, Sasaki K, Ito H et al (2001) A large family of class III plant peroxidases. Plant Cell Physiol 42(5):462–468

    CAS  PubMed  Google Scholar 

  • Hoekenga OA, Vision TJ, Shaff JE et al (2003) Identification and characterization of aluminum tolerance loci in Arabidopsis (Landsberg erecta × Columbia) by quantitative trait locus mapping. A physiologically simple but genetically complex trait. Plant Physiol 132(2):936–948

    CAS  PubMed Central  Google Scholar 

  • Horst WJ, Wang Y, Eticha D (2010) The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminium resistance of plants: a review. Ann Bot 106(1):185–197

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kale SM, Jaganathan D, Ruperao P et al (2015) Prioritization of candidate genes in “QTL-hotspot” region for drought tolerance in chickpea (Cicer arietinum L.). Sci Rep 5:15296

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kereszt A, Li D, Indrasumunar A, et al (2007) Agrobacterium rhizogenes-mediated transformation of soybean to study root biology. Nature protocols 2(4):948

    CAS  PubMed  Google Scholar 

  • Kopittke PM, Moore KL, Lombi E et al (2015) Identification of the primary lesion of toxic aluminum in plant roots. Plant Physiol 167(4):1402–1411

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kopittke PM, Menzies NW, Wang P et al (2016) Kinetics and nature of aluminium rhizotoxic effects: a review. J Exp Bot 67(15):4451–4467

    CAS  PubMed  Google Scholar 

  • Korir PC, Qi B, Wang Y et al (2011) A study on relative importance of additive, epistasis and unmapped QTL for Aluminium tolerance at seedling stage in soybean. Plant Breed 130(5):551–562

    CAS  Google Scholar 

  • Korir PC, Zhang J, Wu K et al (2013) Association mapping combined with linkage analysis for aluminum tolerance among soybean cultivars released in yellow and Changjiang River valleys in China. Theor Appl Genet 126(6):1659–1675

    CAS  PubMed  Google Scholar 

  • Kumar J, Gupta DS, Gupta S et al (2017) Quantitative trait loci from identification to exploitation for crop improvement. Plant Cell Rep 36(8):1187–1213

    CAS  PubMed  Google Scholar 

  • Li X, Li Y, Qu M et al (2016) Cell wall pectin and its methyl-esterification in transition zone determine Al resistance in cultivars of pea (Pisum sativum). Front Plant Sci 7:39

    PubMed  PubMed Central  Google Scholar 

  • Li H, Mollier A, Ziadi N et al (2017) Soybean root traits after 24 years of different soil tillage and mineral phosphorus fertilization management. Soil Tillage Res 165:258–267

    Google Scholar 

  • Li GZ, Wang ZQ, Yokosho K et al (2018) Transcription factor WRKY 22 promotes aluminum tolerance via activation of OsFRDL 4 expression and enhancement of citrate secretion in rice (Oryza sativa). New Phytol 219(1):149–162

    CAS  PubMed  Google Scholar 

  • Little R (1988) Plant soil interactions at low pH problem solving-the genetic approach. Commun Soil Sci Plant Anal 19(7–12):1239–1257

    CAS  Google Scholar 

  • Ma HX, Bai GH, Carver BF et al (2005) Molecular mapping of a quantitative trait locus for aluminum tolerance in wheat cultivar atlas 66. Theor Appl Genet 112(1):51–57

    CAS  PubMed  Google Scholar 

  • Ma Y, Li C, Ryan PR et al (2016) A new allele for aluminium tolerance gene in barley (Hordeum vulgare L.). BMC Genomics 17(1):186

    PubMed  PubMed Central  Google Scholar 

  • Men Y, Wang D, Li B et al (2018) Effects of drought stress on the antioxidant system, osmolytes and secondary metabolites of Saposhnikovia divaricata seedlings. Acta Physiol Plant 40(11):191

    Google Scholar 

  • Meng L, Wang B, Zhao X et al (2017) Association mapping of ferrous, zinc, and aluminum tolerance at the seedling stage in indica rice using MAGIC populations. Front Plant Sci 8:1822

    PubMed  PubMed Central  Google Scholar 

  • Mugwira LM, Elgawhary SM, Patel SU (1978) Aluminium tolerance in triticale, wheat and rye as measured by root growth characteristics and aluminium concentration. Plant Soil 50(1–3):681–690

    CAS  Google Scholar 

  • Pandey S, Ceballos H, Magnavaca R et al (1994) Genetics of tolerance to soil acidity in tropical maize. Crop Sci 34(6):1511–1514

    Google Scholar 

  • Passardi F, Cosio C, Penel C et al (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Rep 24(5):255–265

    CAS  PubMed  Google Scholar 

  • Patil G, Do T, Vuong TD et al (2016) Genomic-assisted haplotype analysis and the development of high-throughput SNP markers for salinity tolerance in soybean. Sci Rep 6:19199

    CAS  PubMed  PubMed Central  Google Scholar 

  • Patil G, Vuong TD, Kale S et al (2018) Dissecting genomic hotspots underlying seed protein, oil, and sucrose content in an interspecific mapping population of soybean using high-density linkage mapping. Plant Biotechnol J 16(11):1939–1953

    CAS  PubMed  PubMed Central  Google Scholar 

  • Polle E, Konzak CF, Kattrick JA (1978) Visual detection of Aluminum tolerance levels in wheat by hematoxylin staining of seedling roots 1. Crop Sci 18(5):823–827

    CAS  Google Scholar 

  • Qi B, Korir P, Zhao T et al (2008) Mapping quantitative trait loci associated with aluminum toxin tolerance in NJRIKY recombinant inbred line population of soybean (Glycine max). J Integr Plant Biol 50(9):1089–1095

    CAS  Google Scholar 

  • Rhue RD, Grogan CO, Stockmeyer EW et al (1978) Genetic control of Aluminum tolerance in corn 1. Crop Sci 18(6):1063–1067

    Google Scholar 

  • Richards KD, Schott EJ, Sharma YK et al (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol 116(1):409–418

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ryan PR, Ditomaso JM, Kochian LV (1993) Aluminium toxicity in roots: an investigation of spatial sensitivity and the role of the root cap. J Exp Bot 44(2):437–446

    CAS  Google Scholar 

  • Ryan PR, Tyerman SD, Sasaki T et al (2010) The identification of aluminium-resistance genes provides opportunities for enhancing crop production on acid soils. J Exp Bot 62(1):9–20

    PubMed  Google Scholar 

  • Salinas J G, Gourley L M. (1987) Workshop on Evaluating Sorghum for Tolerance to Al-toxic Tropical Soils in Latin America (1984, Cali, Colombia). Sorghum for acid soils: Proceedings

  • Sánchez PA, Salinas JG (1981) Low-input technology for managing Oxisols and Ultisols in tropical America [M]//Advances in agronomy. Academic Press 34:279–406

    Google Scholar 

  • Sartain J B. (1974) Differential effects of aluminum on top and root growth, nutrient accumulation and nodulation of several soybean varieties [D]. North Carolina State University at Raleigh

  • Schindler DW, Hecky RE (2009) Eutrophication: more nitrogen data needed. Science 324(5928):721–722

    CAS  PubMed  Google Scholar 

  • Sentelhas PC, Battisti R, Câmara GMS et al (2015) The soybean yield gap in Brazil–magnitude, causes and possible solutions for sustainable production. J Agric Sci 153(8):1394–1411

    Google Scholar 

  • Sharma AD, Sharma H, Lightfoot DA (2011) The genetic control of tolerance to aluminum toxicity in the ‘Essex’ by ‘Forrest’ recombinant inbred line population. Theor Appl Genet 122(4):687–694

    CAS  PubMed  Google Scholar 

  • Shigeto J, Tsutsumi Y (2016) Diverse functions and reactions of class III peroxidases. New Phytol 209(4):1395–1402

    CAS  PubMed  Google Scholar 

  • Siecińska J, Nosalewicz A (2016) Aluminium toxicity to plants as influenced by the properties of the root growth environment affected by other co-stressors: a review [M]//reviews of environmental contamination and toxicology volume 243. Springer, Cham, 1–26

    Google Scholar 

  • Tabaldi LA, Cargnelutti D, Gonçalves JF et al (2009) Oxidative stress is an early symptom triggered by aluminum in Al-sensitive potato plantlets. Chemosphere 76(10):1402–1409

    CAS  PubMed  Google Scholar 

  • Tao Y, Niu Y, Wang Y et al (2018) Genome-wide association mapping of aluminum toxicity tolerance and fine mapping of a candidate gene for Nrat1 in rice. PLoS One 13(6):e0198589

    PubMed  PubMed Central  Google Scholar 

  • Valentine MF, De Tar JR, Mookkan M et al (2017) Silencing of soybean raffinose synthase gene reduced raffinose family oligosaccharides and increased true metabolizable energy of poultry feed. Front Plant Sci 8:692

    PubMed  PubMed Central  Google Scholar 

  • Wang J, Raman H, Zhang G et al (2006) Aluminium tolerance in barley (Hordeum vulgare L.): physiological mechanisms, genetics and screening methods. J Zhejiang Univ Sci B 7(10):769–787

    CAS  PubMed  PubMed Central  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • Wang X, Pan Q, Chen F et al (2011) Effects of co-inoculation with arbuscular mycorrhizal fungi and rhizobia on soybean growth as related to root architecture and availability of N and P. Mycorrhiza 21(3):173–181

    PubMed  Google Scholar 

  • Wang S, Basten CJ, Zeng B (2012) Windows QTL cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC. http://statgen.ncsu.edu/qtlcart/WQTLCart.htm. Accessed 20 June 2018

  • Xie Z, Nolan TM, Jiang H et al (2019) AP2/ERF transcription factor regulatory networks in hormone and abiotic stress responses in Arabidopsis. Front Plant Sci 10

  • Yamamoto Y, Kobayashi Y, Devi SR et al (2002) Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiol 128(1):63–72

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yao Y, He RJ, Xie QL et al (2017) ETHYLENE RESPONSE FACTOR 74 (ERF74) plays an essential role in controlling a respiratory burst oxidase homolog D (RbohD)-dependent mechanism in response to different stresses in Arabidopsis. New Phytol 213(4):1667–1681

    CAS  PubMed  Google Scholar 

  • Yu Y, Zhou W, Zhou K et al (2018) Polyamines modulate aluminum-induced oxidative stress differently by inducing or reducing H2O2 production in wheat. Chemosphere 212:645–653

    CAS  PubMed  Google Scholar 

  • Zhao LN, Zhao Q, Ao GM et al (2009) The foxtail millet Si69 gene is a Wali7 (wheat aluminum-induced protein 7) homologue and may function in aluminum tolerance. Chin Sci Bull 54(10):1697–1706

    CAS  Google Scholar 

  • Zhao M, Song J, Wu A et al (2018) Mining beneficial genes for aluminum tolerance within a core collection of rice landraces through genome-wide association mapping with high density SNPs from specific-locus amplified fragment sequencing. Front Plant Sci 9

  • Zhu XF, Shi YZ, Lei GJ et al (2012) XTH31, encoding an in vitro XEH/XET-active enzyme, regulates aluminum sensitivity by modulating in vivo XET action, cell wall xyloglucan content, and aluminum binding capacity in Arabidopsis. Plant Cell 24(11):4731–4747

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu C, Luo N, He M et al (2014) Molecular characterization and expression profiling of the protein disulfide isomerase gene family in Brachypodium distachyon L. PLoS One 9(4):e94704

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the Projects of Science and Technology of Guangzhou (201804020015); the National Key R&D Program of China (2018YFD0201006); the China Agricultural Research System (CARS-04-PS09) and the Research Project of the State Key Laboratory of Agricultural and Biological Resources Protection and Utilization in Subtropics.

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Y. C., T. L., Q. M. and H. N. provided the soybean materials used in this study. P. X., R. L., X. H., Q. L., and Z. C. performed the experiments and date analyses. Q. X. performed QTL mapping. Z. C. and H. N. prepared the manuscript. H. N. planned, supervised and financed this work, as well as edited the manuscript. All authors have read and approved the final version of the manuscript to be published.

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Correspondence to Hai Nian.

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Cai, Z., Cheng, Y., Xian, P. et al. Fine-mapping QTLs and the validation of candidate genes for Aluminum tolerance using a high-density genetic map. Plant Soil 444, 119–137 (2019). https://doi.org/10.1007/s11104-019-04261-0

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