|Genome-wide association and linkage mapping strategies reveal genetic loci and candidate genes of phosphorus utilization in soybean
|ZHANG Hua*, WU Hai-yan*, TIAN Rui, KONG You-bin, CHU Jia-hao, XING Xin-zhu, DU Hui, JIN Yuan, LI Xi-huan, ZHANG Cai-ying
|State Key Laboratory of North China Crop Improvement and Regulation/Hebei Agricultural University, Baoding 071001, P.R.China
Insufficient available phosphorus in soil has become an important limiting factor for the improvement of yield and quality in soybean. The mining of QTLs and candidate genes controlling soybean phosphorus utilization related traits is a necessary strategy to solve this problem. In this study, 11 phosphorus utilization related traits of a natural population of 281 typical soybean germplasms and a recombinant inbred line (RIL) population of 270 lines were evaluated under different phosphorus conditions at two critical stages: the four-leaf stage as the seedling critical stage was designated as the T1 stage, and the six-leaf stage as the flowering critical stage was designated as the T2 stage. In total, 200 single nucleotide polymorphism (SNP) loci associated with phosphorus utilization related traits were identified in the natural population, including 91 detected at the T1 stage, and 109 detected at the T2 stage. Among these SNP loci, one SNP cluster (s715611375, ss715611377, ss715611379 and ss715611380) on Gm12 was shown to be significantly associated with plant height under the low phosphorus condition at the T1 stage, and the elite haplotype showed significantly greater plant height than the others. Meanwhile, one pleiotropic SNP cluster (ss715606501, ss715606506 and ss715606543) on Gm10 was found to be significantly associated with the ratio of root/shoot, root and total dry weights under the low phosphorus condition at the T2 stage, and the elite haplotype also presented significantly higher values for related characteristics under the phosphorus starvation condition. Furthermore, four co-associated SNP loci (ss715597964, ss715607012, ss715622173 and ss715602331) were identified under the low phosphorus condition at both the T1 and T2 stages, and 12 QTLs were found to be consistent with these genetic loci in the RIL population. More importantly, 14 candidate genes, including MYB transcription factor, purple acid phosphatase, sugar transporter and HSP20-like chaperones superfamily genes, etc., showed differential expression levels after low phosphorus treatment, and three of them were further verified by qRT-PCR. Thus, these genetic loci and candidate genes could be applied in marker-assisted selection or map-based gene cloning for the genetic improvement of soybean phosphorus utilization.
Received: 16 December 2020
Accepted: 01 April 2021
|Fund: This research was funded by the Project of Hebei Province Science and Technology Support Program, China (17927670H and 16227516D-1).
|About author: ZHANG Hua, Mobile: +86-15733202069, E-mail: zhanghua0316@ 163.com; WU Hai-yan, E-mail: email@example.com; Correspondence LI Xi-huan, Tel: +86-312-7528122, E-mail: firstname.lastname@example.org; ZHANG Cai-ying, Tel: +86-312-7521558, E-mail: email@example.com
* These authors contributed equally to this study.
Cite this article:
ZHANG Hua, WU Hai-yan, TIAN Rui, KONG You-bin, CHU Jia-hao, XING Xin-zhu, DU Hui, JIN Yuan, LI Xi-huan, ZHANG Cai-ying.
Genome-wide association and linkage mapping strategies reveal genetic loci and candidate genes of phosphorus utilization in soybean. Journal of Integrative Agriculture, 21(9): 2521-2537.
| Akond M, Liu S M, Schoener L, Anderson J A, Kantartzi S K, Meksem K, Song Q J, Wang D C, Wen Z X, Lightfoot D A, Kassem M A. 2013. A SNP-based genetic linkage map of soybean using the SoySNP6K Illumina Infinium BeadChip genotyping array. Journal of Plant Genome Sciences, 1, 80–89.
Balzergue C, Dartevelle T, Godon C, Laugier E, Meisrimler C, Teulon J M, Creff A, Bissler M, Brouchoud C, Hagège A, Müller J, Chiarenza S, Javot H, Becuwe-Linka N, David P, Péret B, Delannoy E, Thibaud M C, Armengaud J, Abel S, Pellequer J L, Nussaume L, Desnos T. 2017. Low phosphate activates STOP1-ALMT1 to rapidly inhibit root cell elongation. Nature Communications, 8, 15300.
Bilyeu K D, Zeng P Y, Coello P, Zhang Z Y J, Krishnan H B, Bailey A, Beuselinck P R, Polacco J C. 2008. Quantitative conversion of phytate to inorganic phosphorus in soybean seeds expressing a bacterial phytase. Plant Physiology, 146, 468–477.
Bradbury P J, Zhang Z W, Kroon D E, Casstevens T M, Ramdoss Y, Buckler E S. 2007. TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics, 23, 2633–2635.
Cai Z D, Cheng Y B, Xian P Q, Ma Q B, Wen K, Xia Q J, Zhang G Y, Nian H. 2018. Acid phosphatase gene GmHAD1 linked to low phosphorus tolerance in soybean, through fine mapping. Theoretical and Applied Genetics, 131, 1715–1728.
Cui S Y, Geng L Y, Meng Q C, Du D Y. 2007. QTL mapping of phosphorus deficiency tolerance in soybean (Glycine max L.) during seedling stage. Acta Agronomica Sinica, 33, 378–383. (in Chinese)
Evanno G, Regnaut S, Goudet J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Molecular Ecology, 14, 2611–2620.
Gai J Y. 2000. Methods of Experimental Statistics. China Agriculture Press, China. (in Chinese)
Geng L Y, Cui S Y, Zhang D, Xing H, Gai J Y, Yu D Y. 2007. QTL mapping and epistasis analysis for P-efficiency in soybean [Glycine max (L.)]. Soybean Science, 26, 460–466. (in Chinese)
George T S, Richardson A E. 2008. Potential and limitations to improving crops for enhanced phosphorus utilization. Plant Ecophysiology, 7, 247–270.
Gibbs D J, Voß U, Harding S A, Fannon J, Moody L A, Yamada E, Swarup K, Nibau C, Bassel G W, Choudhary A, Lavenus J, Bradshaw S J, Stekel D J, Bennett M J, Coates J C. 2014. AtMYB93 is a novel negative regulator of lateral root development in Arabidopsis. New Phytologist, 203, 1194–1207.
Huo X B, Li X H, Du H, Kong Y B, Tian R, Li W L, Zhang C Y. 2019. Genetic loci and candidate genes of symbiotic nitrogen fixation-related characteristics revealed by a genome-wide association study in soybean. Molecular Breeding, 39, 127.
Hwang E Y, Song Q J, Jia G F, Specht J E, Hyten D L, Costa J, Cregan P B. 2014. A genome-wide association study of seed protein and oil content in soybean. BMC Genomics, 15, 1.
Ju M, Zhou Z J, Mu C, Zhang X C, Gao J Y, Liang Y K, Chen J F, Wu Y B, Li X P, Wang S W, Wen J J, Yang L M, Wu J Y. 2017. Dissecting the genetic architecture of Fusarium verticillioides seed rot resistance in maize by combining QTL mapping and genome-wide association analysis. Scientific Reports, 7, 46446.
Kong Y B, Li X H, Wang B, Li W L, Du H, Zhang C Y. 2018. The soybean purple acid phosphatase GmPAP14 predominantly enhances external phytate utilization in plants. Frontiers in Plant Science, 9, 292.
Leamy L J, Zhang H Y, Li C B, Chen C Y, Song B H. 2017. A genome-wide association study of seed composition traits in wild soybean (Glycine soja). BMC Genomics, 18, 18.
Liang Q, Cheng X H, Mei M T, Yan X L, Liao H. 2010. QTL analysis of root traits as related to phosphorus efficiency in soybean. Annals of Botany, 106, 223–234.
Liao P, Ros M B H, Gestel N V, Sun Y N, Zhang J, Huang S, Zeng Y J, Wu Z M, Groenigen K J V. 2020. Liming reduces soil phosphorus availability but promotes yield and P uptake in a double rice cropping system. Journal of Integrative Agriculture, 19, 2807–2814.
Li C C, Gui S H, Yang T, Walk T, Wang X R, Liao H. 2012. Identification of soybean purple acid phosphatase genes and their expression responses to phosphorus availability and symbiosis. Annals of Botany, 109, 275–285.
Li H Y, Yang Y M, Zhang H Y, Chu S S, Zhang X G, Yin D M, Yu D Y, Zhang D. 2016. A genetic relationship between phosphorus efficiency and photosynthetic traits in soybean as revealed by QTL analysis using a high-density genetic map. Frontiers in Plant Science, 7, 924.
Li X H, Kamala S, Tian R, Du H, Li W L, Kong Y B, Zhang C Y. 2018. Identification and validation of quantitative trait loci controlling seed isoflavone content across multiple environments and backgrounds in soybean. Molecular Breeding, 38, 8.
Li Y D, Wang Y J, Tong Y P, Gao J G, Zhang J S, Chen S Y. 2005. QTL mapping of phosphorus deficiency tolerance in soybean (Glycine max L. Merr.). Euphytica, 142, 137–142.
Liu M, Tan X L, Yang Y, Liu P, Zhang X X, Zhang Y C, Wang L, Hu Y, Ma L L, Li Z L, Zhang Y L, Zou C Y, Lin H J, Gao S B, Lee M, Lübberstedt T, Pan G T, Shen Y O. 2019. Analysis of the genetic architecture of maize kernel size traits by combined linkage and association mapping. Plant Biotechnology Journal, 18, 207–221.
Liu S L, Cheng Y B, Ma Q B, Li M, Jiang Z, Xia Q J, Nian H. 2021. Fine mapping and genetic analysis of resistance genes, Rsc18, against soybean mosaic virus. Journal of Integrative Agriculture, 20, 2–11.
Meng L, Li H H, Zhang L Y, Wang J K. 2015. QTL IciMapping: Integrated software for genetic linkage map construction and quantitative trait locus mapping in biparental populations. Crop Journal, 3, 269–283.
Mora-Macías J, Ojeda-Rivera J O, Gutiérrez-Alanís D, Yong-Villalobos L, Oropeza-Aburto A, Raya-González J, Jiménez-Domínguez G, Chávez-Calvillo G, Rellán-Álvarez R, Herrera-Estrella L. 2017. Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate. Proceedings of the National Academy of Sciences of the United States of America, 114, E3563–E3572.
Muchhal U S, Pardo J M, Raghothama K G. 1996. Phosphate transporters from the higher plant Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America, 93, 10519–10523.
Mukatira U T, Liu C, Varadarajan D K, Raghothama K G. 2001. Negative regulation of phosphate starvation-induced genes. Plant Physiology, 127, 1854–1862.
Nilsson L, Müller R, Nielsen T H. 2007. Increased expression of the MYB-related transcription factor, PHR1, leads to enhanced phosphate uptake in Arabidopsis thaliana. Plant Cell & Environment, 30, 1499–1512.
Ning L H, Kan G Z, Du W K, Guo S W, Wang Q, Zhang G Z, Cheng H, Yu D Y. 2016. Association analysis for detecting significant single nucleotide polymorphisms for phosphorus-deficiency tolerance at the seedling stage in soybean [Glycine max (L.) Merr]. Breeding Science, 66, 191–203.
Peng W T, Wu W W, Peng J C, Li J J, Lin Y, Wang Y N, Tian J, Sun L L, Liang C Y, Liao H. 2018. Characterization of the soybean GmALMT family genes and the function of GmALMT5 in response to phosphate starvation. Journal of Integrative Plant Biology, 60, 216–231.
Quint M, Barkawi L S, Fan K T, Cohen J D, Gray W M. 2009. Arabidopsis IAR4 modulates auxin response by regulating auxin homeostasis. Plant Physiology, 150, 748–758.
Phansak P, Soonsuwon W, Hyten D L, Song Q J, Cregan P B, Graef G L, Specht J E. 2016. Multi-population selective genotyping to identify soybean [Glycine max (L.) Merr.] seed protein and oil QTLs. G3 Genes/Genomes/Genetics, 6, 1635–1648.
Song Q J, Hyten D L, Jia G F, Quigley C V, Fickus E W, Nelson R L, Cregan P B. 2013. Development and evaluation of SoySNP50K, a high-density genotyping array for soybean. PLoS ONE, 8, e54985.
Su H, Li Z G, Song S H. 2009. Molecular mapping of QTLs major agronomic traits in soybean (Glycine max L.) under phosphorus deficiency stress. Acta Agriculture Boreali-Occidentalis Sinica, 18, 98–101, 116. (in Chinese)
Tang Y, Liu X L, Wang J B, Li M, Wang Q S, Tian F, Su Z B, Pan Y C, Liu D, Lipka A E, Buckler E S, Zhang Z W. 2016. GAPIT version 2: An enhanced integrated tool for genomic association and prediction. Plant Genome, 9, doi: 10.3835/plantgenome2015.11.0120.
Wang L N, Wei B, Hu G, Hu G Z, Wang L, Jin Y, Sun Z G. 2015. Retraction note to: Gene expression analyses to explore the biomarkers and therapeutic targets for gliomas. Neurological Sciences, 36, 403–409.
Wang X R, Wang Y X, Tian J, Lim B L, Yan X L, Liao H. 2009. Overexpressing AtPAP15 enhances phosphorus efficiency in soybean. Plant Physiology, 151, 233–240.
Wu H Y. 2016. Unconditional and conditional QTL mapping of low phosphorus tolerance related traits at seedling stage in soybean. MSc thesis, Hebei Agricultural University, China. (in Chinese)
Wu H Y, Li X H, Li W L, Kong Y B, Du H, Zhang C Y. 2020. Identification of low phosphorus tolerant traits and selection of elite genotypes in soybean. Journal of Henan Agricultural Sciences, 49, 61–67. (in Chinese)
Wu P, Wang X M. 2008. Role of OsPHR2 on phosphorus homeostasis and root hairs development in rice (Oryza sativa L.). Plant Signaling & Behavior, 3, 674–675.
Yang Y Q, Tong Y, Li X X, He Y, Xu R N, Liu D, Yang Q, Lv H Y, Liao H. 2019. Genetic analysis and fine mapping of phosphorus efficiency locus 1 (PE1) in soybean. Theoretical and Applied Genetics, 132, 2847–2858.
Yao Z F, Tian J, Liao H. 2014. Comparative characterization of GmSPX members reveals that GmSPX3 is involved in phosphate homeostasis in soybean. Annals of Botany, 114, 477–488.
Zhang D, Cheng H, Geng L Y, Kan G Z, Cui S Y, Meng Q C, Gai J Y, Yu D Y. 2009. Detection of quantitative trait loci for phosphorus deficiency tolerance at soybean seedling stage. Euphytica, 167, 313–322.
Zhang D, Li H Y, Wang J S, Zhang H Y, Hu Z B, Chu S S, Lv H Y, Yu D Y. 2016. High-density genetic-mapping identifies new major loci for tolerance to low-phosphorus stress in soybean. Frontiers in Plant Science, 7, 372.
Zhang D, Liu C, Cheng H, Kan G, Cui S, Meng Q, Gai J, Yu D. 2010. Quantitative trait loci associated with soybean tolerance to low phosphorus stress based on flower and pod abscission. Plant Breeding, 129, 243–249.
Zhang D, Song H N, Cheng H, Hao D R, Wang H, Kan G Z, Jin H X, Yu D Y. 2014. The acid phosphatase-encoding gene GmACP1 contributes to soybean tolerance to low-phosphorus stress. PLoS Genetics, 10, e1004061.
Zhang H, Tian R, Chu J H, Xing X Z, Chen S L, Li X H, Zhang C Y. 2020. Mining of genetic loci controlling phosphorus efficiency at crucial phosphorus requirement stages in soybean. Journal of Plant Genetic Resources, 4, 991–1001. (in Chinese)
Zhang J, Gu M, Liang R S H, Shi X Y, Chen L L, Hu X, Wang S C, Dai X L, Qu H Y, Li H H, Xu G H. 2021. OsWRKY21 and OsWRKY108 function redundantly to promote phosphate accumulation through maintaining the constitutive expression of OsPHT1;1 under phosphate-replete conditions. New Phytologist, 229, 1598–1614.
Zhang W, Liao X L, Cui Y M, Ma W Y, Zhang X N, Du H Y, Ma Y J, Ning L H, Wang H, Huang F, Yang H, Kan G Z, Yu D Y. 2019. A cation diffusion facilitator, GmCDF1, negatively regulates salt tolerance in soybean. PLoS Genetics, 15, e1007798.
|No Suggested Reading articles found!