An Integrated Quantitative Trait Locus Map of Oil Content in Soybean, Glycine max (L.) Merr., Generated Using a Meta-Analysis Method for Mining Genes

doi:10.1016/S1671-2927(11)60166-1

Journal of Integrative Agriculture ›› 2011, Vol. 10 ›› Issue (11): 1681-1692.DOI: 10.1016/S1671-2927(11)60166-1

An Integrated Quantitative Trait Locus Map of Oil Content in Soybean, Glycine max (L.) Merr., Generated Using a Meta-Analysis Method for Mining Genes

QI Zhao-ming, HAN Xue, SUN Ya-nan, WU Qiong, SHAN Da-peng, DU Xiang-yu, LIU Chun-yan, JIANG Hong-wei, HU Guo-hua , CHEN Qing-shan

1.Soybean Research Institute, Northeast Agricultural University
2.Crop Research and Breeding Center of Land-Reclamation
3.Heilongjiang Academy of Agricultural Sciences, Suihua Institute

收稿日期:2010-06-25 出版日期:2011-11-01 发布日期:2011-11-07
通讯作者: Correspondence HU Guo-hua, Professor, Tel: +86-451-55191945, E-mail: hugh757@vip.163.com; CHEN Qing-shan, Professor, Tel: +86-451-55191945, E-mail: qshchen@126.com
作者简介:QI Zhao-ming, Ph D, E-mail: qizhaoming1860@126.com
基金资助:
This study was supported by the Transgenic Specific Technology Programs, China (2009ZX08009-013B).

An Integrated Quantitative Trait Locus Map of Oil Content in Soybean, Glycine max (L.) Merr., Generated Using a Meta-Analysis Method for Mining Genes

QI Zhao-ming, HAN Xue, SUN Ya-nan, WU Qiong, SHAN Da-peng, DU Xiang-yu, LIU Chun-yan, JIANG Hong-wei, HU Guo-hua , CHEN Qing-shan

1.Soybean Research Institute, Northeast Agricultural University
2.Crop Research and Breeding Center of Land-Reclamation
3.Heilongjiang Academy of Agricultural Sciences, Suihua Institute

Received:2010-06-25 Online:2011-11-01 Published:2011-11-07
Contact: Correspondence HU Guo-hua, Professor, Tel: +86-451-55191945, E-mail: hugh757@vip.163.com; CHEN Qing-shan, Professor, Tel: +86-451-55191945, E-mail: qshchen@126.com
About author:QI Zhao-ming, Ph D, E-mail: qizhaoming1860@126.com
Supported by:
This study was supported by the Transgenic Specific Technology Programs, China (2009ZX08009-013B).

摘要/Abstract

摘要： Soybean is a major cash crop in the world, and its oil content was one of the very important traits. Therefore, the study of gene mapping for oil content in soybean is very important for breeding application. At present, at least 130 QTL loci for soybean oil content have been published; however, the mapping results of oil content were dispersed and a coalescent public map should be established to integrate the published QTLs, and to more efficiently mine genes based on the metaanalysis method of the bioinformatics tools. This study was to construct an integrated map of QTLs for soybean oil content and accelerate the application of bioinformation resource related to oil content improvement in the practice of soybean breeding. We collected information of 130 QTLs reported over the past 20 yr for soybean oil content and used the Software BioMercator 2.1 to project QTLs from their own maps onto a reference map, which was an early-integrated map constructed by Song (2004) for oil-content quantitative trait loci (QTLs) in soybean. Gene mining was performed based on the meta-analysis by running the local ver. GENSCAN and InterProScan. The confidence interval of QTLs was efficaciously narrowed using the meta-analysis method, and 25 consensus QTLs were mapped on the reference map. Using a local version of GENSCAN, 12 805 sequences in the consensus QTL intervals were predicted. With BLAST, these predicted sequences were aligned to gene sequences from the International Protein Index database using InterProScan locally. Thirteen predicted genes were in the class of the geme ontology (GO) accession (0006631), which were involved in the fatty acid metabolic process. These genes were analyzed using BLAST at the NCBI website to examine whether they were related to oil content. Six genes were found in the oil-synthesis pathway. Twenty-five consensus QTLs and six genes were found in the oil-synthesis pathway. These results would lay the foundation for marker-assisted selection and mapping QTL precisely, and these genes will facilitate the researches on the gene mining of oil synthesis and molecular breeding in soybean.

关键词: soybean, oil content, meta-analysis, consensus QTL, gene ontology (GO)

Abstract: Soybean is a major cash crop in the world, and its oil content was one of the very important traits. Therefore, the study of gene mapping for oil content in soybean is very important for breeding application. At present, at least 130 QTL loci for soybean oil content have been published; however, the mapping results of oil content were dispersed and a coalescent public map should be established to integrate the published QTLs, and to more efficiently mine genes based on the metaanalysis method of the bioinformatics tools. This study was to construct an integrated map of QTLs for soybean oil content and accelerate the application of bioinformation resource related to oil content improvement in the practice of soybean breeding. We collected information of 130 QTLs reported over the past 20 yr for soybean oil content and used the Software BioMercator 2.1 to project QTLs from their own maps onto a reference map, which was an early-integrated map constructed by Song (2004) for oil-content quantitative trait loci (QTLs) in soybean. Gene mining was performed based on the meta-analysis by running the local ver. GENSCAN and InterProScan. The confidence interval of QTLs was efficaciously narrowed using the meta-analysis method, and 25 consensus QTLs were mapped on the reference map. Using a local version of GENSCAN, 12 805 sequences in the consensus QTL intervals were predicted. With BLAST, these predicted sequences were aligned to gene sequences from the International Protein Index database using InterProScan locally. Thirteen predicted genes were in the class of the geme ontology (GO) accession (0006631), which were involved in the fatty acid metabolic process. These genes were analyzed using BLAST at the NCBI website to examine whether they were related to oil content. Six genes were found in the oil-synthesis pathway. Twenty-five consensus QTLs and six genes were found in the oil-synthesis pathway. These results would lay the foundation for marker-assisted selection and mapping QTL precisely, and these genes will facilitate the researches on the gene mining of oil synthesis and molecular breeding in soybean.

Key words: soybean, oil content, meta-analysis, consensus QTL, gene ontology (GO)

QI Zhao-ming, HAN Xue, SUN Ya-nan, WU Qiong, SHAN Da-peng, DU Xiang-yu, LIU Chun-yan, JIANG Hong-wei, HU Guo-hua , CHEN Qing-shan . An Integrated Quantitative Trait Locus Map of Oil Content in Soybean, Glycine max (L.) Merr., Generated Using a Meta-Analysis Method for Mining Genes [J]. Journal of Integrative Agriculture, 2011, 10(11): 1681-1692.

参考文献

[1]Arcade A, Labourdette A, Falque M, Mangin B, Chardon F, Charcosset A, Joets J. 2004. Biomercator: integrating genetic maps and QTL towards discovery of candidate genes. Bioinformatics, 20, 2324-2326.

[2]Brummer E C, Graef G L, Orf J, Wilcox J R, Shoemaker R C. 1997. Mapping QTL for seed protein and oil content in eight soybean populations. Crop Science, 37, 370-378.

[3]Buchanan B, Gruissem W, Jones R L. 2000. Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists, Rockville, Maryland. pp. 456-526.

[4]Chardon F, Virlon B, Moreau L, Falque M, Joets J, Decousset L, Murigneux A, Charcosset A. 2004. Genetic architecture of flowering time in maize as inferred from quantitative trait loci meta-analysis and synteny conservation with the rice genome. Genetics, 168, 2169-2185.

[5]Chen Q S, Zhang Z C, Liu C Y, Xin D W, Shan D P, Qiu H M, Shan C Y. 2007. QTL mapping of some agronomic traits of soybean. Agricultural Sciences in China, 6, 399-405.

[6]Chung J, Babka H L, Graef G L, Staswick P E, Lee D J, Cregan P B, Shoemaker R C, Specht J E. 2003. The seed protein, oil, and yield QTL on soybean linkage group I. Crop Science, 43, 1053-1067.

[7]Csanádi G, Vollmann J, Stift G, Lelley T. 2001. Seed quality QTLs identified in a molecular map of early maturing soybean. Theoretical and Applied Genetics, 103, 912-919.

[8]Darvasi A, Soller M. 1997. A simple method to calculate resolving power and confidence interval of QTL map location. Behavioral Genetics, 27, 125-132.

[9]Diers B W, Keim P, Fehr W R, Shoemaker R C. 1992. RFLP analysis of soybean seed protein and oil content. Theoretical and Applied Genetics, 83, 608-612.

[10]Fasoula V A, Harris D K, Boerma H R. 2004. Vaidation and designation of quantitative trait loci for seed protein, seed oil and seed weight from two soybean population. Crop Science, 44, 1218-1225.

[11]Goffinet B, Gerber S. 2000. Quantitative trait loci: a metaanalysis. Genetics, 155, 463-473.

[12]Guo B, Sleper D A, Lu P, Shannon J G, Nguyen H T, Arelli P R. 2006. QTLs associated with resistance to soybean cyst nematode in soybean: meta-analysis of QTL location. Crop Science, 46, 595-602.

[13]Hanocq E, Laperche A, Jaminon O, Lainé A L, le Gouis J. 2007. Most significant genome regions involved in the control of earliness traits in bread wheat, as revealed by QTL metaanalysis. Theoretical and Applied Genetics, 114, 569-584.

[14]Heppard E P, Kinney A J, Stecca K L, Miao G H. 1996. Developmental and growth temperature regulation of two different microsomal omega-6 desaturase genes in soybeans. Plant Physiology, 110, 311-319.

[15]Hyten D L, Pantalone V R, Sams C E, Saxton A M, Landau-Ellis D, Stefaniak T R, Schmidt M E. 2004. Seed quality QTL in a prominent soybean population. Theoretical and Applied Genetics, 109, 552-561.

[16]Ji H L, Li X H, Xie C X, Hao Z F, Lv X L, Shi L Y, Zhang S H. 2007. Comparative QTL mapping of resistance to Sporisorium reiliana in maize based on meta-analysis of QTL locations. Journal of Plant Genetic Resources, 8, 132-139.

[17]Kabelka E A, Diers B W, Fehr W R, LeRoy A R, Baianu I C, You T, Neece D J, Nelson R L. 2004. Putative alleles for increased yield from soybean plant introduction. Crop Science, 44, 784-791.

[18]Kang M S. 1998. Using genotype-by-environment interaction for crop cultivar development. Advances in Agronomy, 35, 199-240.

[19]Lanaud C, Fouet O, Clement D, Boccara M, Risterucci A M, Legavre T, Surujdeo-Maharaj S, Argout X. 2009. A metaQTL analysis of disease resistance traits of Theobroma cacao L. Molecular Breeding, 24, 361-374.

[20]Wang Y G, Deng Q Y, Liang F S, Xing Q H, Li J M, Xiong Y D, Sun S M, Guo B T, Yuan L P, Wang B. 2004. Molecular marker assisted selection for yield enhancing genes in the progeny of Minghui 639 Qrufipogon. Agricultural Sciences in China, 3, 89-93.

[21]Lander E, Kruglyak L. 1995. Genetic dissection of complex traits: Guidelines for interpreting and reporting linkage results. Nature Genetics, 11, 241-247.

[22]Lee S H, Mian M A R, Carter T E, Shipe E R, Ashley D A, Parrott W A, Hussey R S, Boerma H R, Bailey M A. 1996. RFLP loci associated with soybean seed protein and oil content across populations and locations. Theoretical and Applied Genetics, 93, 649-657.

[23]Li X H, Li X H, Hao Z F, Tian Q Z, Zhang S H. 2005. Consensus map of the QTL relevant to drought tolerance of maize under drought conditions. Scientia Agricultura Sinica, 38, 882-890. (in Chinese)

[24]Li Q. 2004. Targeting and mapping of protein and oil content related genes by SSR markers in soybean. MSc thesis, Nanjing Agricultural University. (in Chinese)

[25]Liang S Q. 2005. Analysis by QTL for protein and oil content of soybean seed. MSc thesis, Guangxi University. (in Chinese)

[26]Lv X L, Li X H, Xie C X, Hao Z F, Ji H L, Shi L Y, Zhang S H. 2008. Comparative QTL mapping of resistance to sugarcane mosaic virus in maize based on bioinformatics. Hereditas, 30, 101-108.

[27]Lv Z Z. 2006. Construction of soybean genetic map, QTL mapping of agronomic traits, and identification on excellent gene. Ph D thesis, Shandong Agricultural University. (in Chinese)

[28]Mansur L M, Lark K G, Kross H, Oliveira A. 1993. Interval mapping of quantitative trait loci for reproductive, morphological, and seed traits of soybean (Glycine max L.). Theoretical and Applied Genetics, 86, 907-913.

[29]Mansur L M, Orf J H, Chase K, Jarvik T, Cregan P B, Lark K G. 1996. Genetic mapping of agronomic traits using recombinant inbred lines of soybean. Crop Science, 36, 1327-1336.

[30]Orf J H, Chase K, Jarvik T, Mansur L M, Cregan P B, Adler F R, Lark K G. 1999. Genetics of soybean agronomic traits: I. Comparison of three related recombinant inbred populations. Crop Science, 39, 1642-1651.

[31]Panthee D R, Pantalone V R, West D R, Saxton A M, Sams C E. 2005. Quantitative trait loci for seed protein and oil concentration, and seed size in soybean. Crop Science, 45, 2015-2022.

[32]Paterson A H, Lander E S, Hewitt J D, Peterson S, Lincoln S E, Tanksley S D. 1988. Resolution of quantitative traits into Mendelian factors by using a complete linkage map of restriction fragment length polymorphisms. Nature, 335, 721726.

[33]Qiu B X, Arelli P R, Sleper D A. 1999. RFLP markers associated with soybean cyst nematode resistance and seed composition in a ‘Peking’×‘Essex’ population. Theoretical and Applied Genetics, 98, 356-364.

[34]Ren B, Li Y. 2005. Research advances on fatty acid biogynthesis metabolism in soybean seed. Molecular Plant Breeding, 3, 301-306.

[35]Romagosa I, Han F, Ullrich S E, Hayes P M, Wesenberg D M. 1999. Verification of yield QTL through realized molecular marker-assisted selection responses in a barley cross. Molecular Breeding, 5, 143-152.

[36]Rong J K, Feltus F A, Waghmare V N, Pierce G J, Chee P W, Draye X, Saranga Y, Wright R J, Wilkins T A, May O L, et al. 2007. Meta-analysis of polyploid cotton QTL shows unequal contributions of subgenomes to a complex network of genes and gene clusters implicated in lint fiber development. Genetics, 176, 2577-2588.

[37]Rudner L M, Glass G V, Evartt D L, Emery P J. 2002. A user’s Guide to the Meta-Analysis of Research Studies: Meta-Stat, Software to Aid in the Meta-Analysis of Research Findings. Educational Resources Information Center, Clearinghouse on Assessment and Evaluation, University of Maryland, College Park, MD.

[38]Sebolt A M, Shoemaker R C, Diers B W. 2000. Analysis of a quantitative trait locus allele from wild soybean that increases seed protein concentration in soybean. Crop Science, 40, 1438-1444.

[39]Shan D P, Qi Z M, Qiu H M, Shan C Y, Liu C Y, Hu G H, Chen Q S. 2008. Epistatic effects of QTLs and QE interaction effects on oil content in soybean. Acta Agronomica Sinica, 34, 952-957.

[40]Shi D Q, Zhou Y H, Chen Z H. 2002. Manipulation of plant fatty acid. Chinese Bulletin of Sciences, 14, 291-296.

[41]Shi L Y, Li X H, Hao Z F, Xie C X, Ji H L, Lv X L, Zhang S H, Pan G T. 2007. Comparative QTL mapping of resistance to gray leaf spot in maize based on bioinformatics. Agricultural Sciences in China, 6, 1411-1419.

[42]Smith K J, Huyser W. 1987. World distribution and significance of soybean. In: Wilcox J R, ed., Soybeans: Improvement, Production, and Uses. 2nd ed. American Society of Agronomy, Madison, WI, USA. pp. 23-48.

[43]Somerville C, Browse J, Jaworski J G, Ohlrogge J. 2000. Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists. pp. 456-527.

[44]Song Q J, Marek L F, Shoemaker R C, Lark K G, Concibido V C, Delannay X, Specht J E, Cregan P B. 2004. A new integrated genetic linkage map of the soybean. Theoretical and Applied Genetics, 109, 122-128.

[45]Specht J E, Chase K, Macrander M, Graef G L, Chung J, Markwell J P, Germann M, Orf J H, Lark K G. 2001. Soybean response to water: a QTL analysis of drought tolerance. Crop Science, 41, 493-509.

[46]Tajuddin T, Watanabe S, Yamanaka N. 2003. Analysis of quantitative trait loci for protein and lipid contents in soybean seeds using recombinant inbred lines. Breeding Science, 53, 133-140.

[47]Thomson M J, Tai T H, McClung A M, Lai X H, Hinga M E, Lobos K B, Xu Y, Martinez C P, McCouch S R. 2003. Mapping quantitative trait loci for yield, yield components and morphological traits in an advanced backcross population between Oryza rufipogon and the Oryza sativa cultivar Jefferson. Theoretical and Applied Genetics, 107, 479-493.

[48]Wang Y G, Deng Q Y, Liang F S, Xing Q H, Li J M, Xiong Y D, Sun S M, Guo B T, Yuan L P, Wang B. 2004. Molecular marker assisted selection for yield enhancing genes in the progeny of Minghui 639 O. rufipogon. Agricultural Sciences in China, 3, 89-93.

[49]Wang Y J. 2001. Establishment and adjustment of RIL population and its application to map construction, mapping genes resistant to SMV and QTL analysis of agronomic and quality traits in soybeans. Ph D thesis, Nanjing Agricultural University. (in Chinese)

[50]Wang X S, Paigen B. 2002. Quantitative trait loci and candidate genes regulating HDL cholesterol: a murine chromosome map. Arteriosclerosis,Thrombosis, and Vascular Biology, 22, 1390-1401.

[51]Wang X Z, Zhou R, Zhang X J, Shan Z H, Sha A H, Chen H F, Qiu D Z, Li P W, Zhou X A. 2008. Map construction and QTL analysis of oil content in soybean. Chinese Journal of Oil Crop Science, 30, 272-278. (in Chinese)

[52]Wang Y, Yao J, Zhang Z F, Zheng Y L. 2006. The comparative analysis based on maize integrated QTL map and metaanalysis of plant height QTLs. Chinese Science Bulletin, 51, 2219-2230.

[53]Warthmann N, Das S, Lanz C, Weigel D. 2008. Comparative analysis of the MIR319a microRNA locus in Arabidopsis and related Brassicaceae. Molecular Biology and Evolution, 25, 892-902.

[54]Wu X L, Wang Y J, He C Y, Chen S Y, Gai J Y, Wang X C. 2001. QTL mapping of some agronomic traits of soybean. Hereditas, 28, 947-955.

[55]Xu P, Wang H, Li Q, Gai J Y, Yu D Y. 2007. QTL positioning of oil content in soybean. Hereditas, 29, 92-96.

[56]Yang Z, Guan R X, Wang Y Q, Liu Z X, Chang R Z, Wang S M, Qiu L J. 2004. Construction of genetic map and QTL analysis for some agronomic traits in soybean. Acta Agronomica Sinica, 30, 413-418.

[57]Zhang W K, Wang Y J, Luo G Z, Zhang J S, He C Y, Wu X L, Gai J Y, Chen S Y. 2004. QTL mapping of ten agronomic traits on the soybean (Glycine max L. Merr.) genetic map and their association with EST markers. Theoretical and Applied Genetics, 108, 1131-1139.

[58]Zhang Z C, Zhan X L, Chen Q S, Teng W L, Yang Q K, Li W B. 2004. QTL mapping seed oil and protein content of soybean. Soybean Science, 23, 81-85.

[59]Zhang X M. 2004. Genetic diversity and QTL analysis of soybean germplasm in Russia and China. MSc thesis, Northeast Agricultural University. (in Chinese)

[60]Zhu X L. 2006. Constructing of genetic linkage map and QTL mapping of important agronomic traits in two soybean populations. MSc thesis, Northeast Agricultural University. (in Chinese)

An Integrated Quantitative Trait Locus Map of Oil Content in Soybean, Glycine max (L.) Merr., Generated Using a Meta-Analysis Method for Mining Genes

An Integrated Quantitative Trait Locus Map of Oil Content in Soybean, Glycine max (L.) Merr., Generated Using a Meta-Analysis Method for Mining Genes

PDF

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 15

编辑推荐

Metrics

[1]	KONG Ling-an, WU Du-qing, HUANG Wen-kun, PENG Huan, HE Wen-ting, PENG De-liang. Assaying the potential of twenty-one legume plants in Medicago truncatula and M. sativa for candidate model plants for investigation the interactions with Heterodera glycines[J]. Journal of Integrative Agriculture, 2016, 15(3): 702-704.
[2]	LI Yan-fei, HONG Hui-long, LI Ying-hui, MA Yan-song, CHANG Ru-zhen, QIU Li-juan. The identification of presence/absence variants associated with the apparent differences of growth period structures between cultivated and wild soybeans[J]. Journal of Integrative Agriculture, 2016, 15(2): 262-270.
[3]	ZHANG Li-wei, Til Feike, Jirko Holst, Christa Hoffmann, Reiner Doluschitz. Comparison of energy consumption and economic performance of organic and conventional soybean production - A case study from Jilin Province, China[J]. Journal of Integrative Agriculture, 2015, 14(8): 1561-1572.
[4]	GUO Bing-fu, GUO Yong, WANG Jun, ZHANG Li-juan, JIN Long-guo, HONG Hui-long, CHANG, Ru-zheng, QIU Li-juan. Co-treatment with surfactant and sonication significantly improves Agrobacterium-mediated resistant bud formation and transient expression efficiency in soybean[J]. Journal of Integrative Agriculture, 2015, 14(7): 1242-1250.
[5]	ZHOU De, Dieter Koemle. Price transmission in hog and feed markets of China[J]. Journal of Integrative Agriculture, 2015, 14(6): 1122-1129.
[6]	CHEN Hua-tao, CHEN Xin, WU Bing-yue, YUAN Xing-xing, ZHANG Hong-mei, CUI Xiao-yan. Whole-genome identification and expression analysis of K+ efflux antiporter (KEA) and Na+/H+ antiporter (NHX) families under abiotic stress in soybean[J]. Journal of Integrative Agriculture, 2015, 14(6): 1171-1183.
[7]	WANG Xiao-guang, ZHAO Xin-hua, JIANG Chun-ji, LI Chun-hong, CONG Shan, WU Di, CHEN Yan-qiu, YU Hai-qiu, WANG Chun-yan. Effects of potassium deficiency on photosynthesis and photoprotection mechanisms in soybean (Glycine max (L.) Merr.)[J]. Journal of Integrative Agriculture, 2015, 14(5): 856-863.
[8]	WU Ting-ting, LI Jin-yu, WU Cun-xiang, SUN Shi, MAO Ting-ting, JIANG Bing-jun, HOU Wen-sheng, HAN Tian-fu. Analysis of the independent- and interactive-photo-thermal effects on soybean flowering[J]. Journal of Integrative Agriculture, 2015, 14(4): 622-632.
[9]	DONG Yong-bin, ZHANG Zhong-wei, SHI Qing-ling, WANG Qi-lei, ZHOU Qiang, DENG Fei, MA Zhi-yan, QIAO Da-he, LI Yu-ling. QTL consistency for agronomic traits across three generations and potential applications in popcorn[J]. Journal of Integrative Agriculture, 2015, 14(12): 2547-2557.
[10]	WANG Jun, LIU Lin, GUO Yong, WANG Yong-hui, ZHANG Le, JIN Long-guo, GUAN Rong-xia, LIU Zhang-xiong, WANG Lin-lin, CHANG Ru-zhen , QIU Li-juan. A Dominant Locus, qBSC-1, Controls β Subunit Content of Seed Storage Protein in Soybean (Glycine max (L.) Merri.)[J]. Journal of Integrative Agriculture, 2014, 13(9): 1854-1864.
[11]	AO Xue, GUO Xiao-hong, ZHU Qian, ZHANG Hui-jun, WANG Hai-ying, MA Zhao-hui, HAN, Xiao-ri, ZHAO Ming-hui , XIE Fu-ti. Effect of Phosphorus Fertilization to P Uptake and Dry Matter Accumulation in Soybean with Different P Efficiencies[J]. Journal of Integrative Agriculture, 2014, 13(2): 326-334.
[12]	ZHANG Gu-wen, XU Sheng-chun, HU Qi-zan, MAO Wei-hua , GONG Ya-ming. Putrescine Plays a Positive Role in Salt-Tolerance Mechanisms by Reducing Oxidative Damage in Roots of Vegetable Soybean[J]. Journal of Integrative Agriculture, 2014, 13(2): 349-357.
[13]	LI Xi-huan, WANG Yun-jie, WU Bing, KONG You-bin, LI Wen-long, CHANG Wen-suo , ZHANG Cai-ying. GmPHR1, a Novel Homolog of the AtPHR1 Transcription Factor, Plays a Role in Plant Tolerance to Phosphate Starvation[J]. Journal of Integrative Agriculture, 2014, 13(12): 2584-2593.
[14]	LI Bin, SUN Jun-ming, WANG Lan, ZHAO Rong-juan , WANG Lian-zheng. Comparative Analysis of Gene Expression Profiling Between Resistant and Susceptible Varieties Infected With Soybean Cyst Nematode Race 4 in Glycine max[J]. Journal of Integrative Agriculture, 2014, 13(12): 2594-2607.
[15]	Zheng gui-jie, Yang Yong-qing, Ma Ying, Yang Xiao-feng, Chen Shan-yu, Ren Rui, Wang Da-gang, Yang Zhong-lu , ZhI hai-jian. Fine Mapping and Candidate Gene Analysis of Resistance Gene RSC3Q to Soybean mosaic virus in Qihuang 1[J]. Journal of Integrative Agriculture, 2014, 13(12): 2608-2615.