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Journal of Integrative Agriculture  2018, Vol. 17 Issue (12): 2734-2744    DOI: 10.1016/S2095-3119(18)62105-7
Special Issue: 线虫合辑Nematology
Plant Protection Advanced Online Publication | Current Issue | Archive | Adv Search |
Chemical mutagenesis and soybean mutants potential for identification of novel genes conferring resistance to soybean cyst nematode
GE Feng-yong1, ZHENG Na1, ZHANG Liu-ping1, HUANG Wen-kun1, PENG De-liang1, LIU Shi-ming1, 2
1 Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China
2 College of Plant Protection, Hunan Agricultural University, Changsha 410128, P.R.China
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Abstract  
The resistance of soybean (Glycine max (L.) Merr.) to soybean cyst nematode (SCN, Heterodera glycines Ichinohe), which is a devastating pathogen in soybean production and causes a large quantity of annual yield loss worldwide, can shift during the long-term interaction and domestication.  It is vital to identify more new resistance genetic sources for identification of novel genes underlying resistance to SCN for management of this pathogen.  In the present study, first, two ethane methylsulfonate-mutagenesis soybean M2 populations of PI 437654, which shows a broad resistance to almost all of SCN races, and Zhonghuang 13, which is a soybean cultivar in China conferring strong resistance to lodging, were developed.  Many types of morphological phenotypes such as four- and five-leaflet leaves were observed from these two soybean M2 populations.  Second, 13 mutants were identified and confirmed to exhibit alteration of resistance to SCN race 4 through the forward genetic screening of 400 mutants of the PI 437654 M2 population, the rate of mutants with alteration of SCN-infection phenotype is 3.25%.  Third, these identified mutants were further verified not to show any changes in the genomic sequences of the three known SCN-resistant genes, GmSHMT08, GmSNAP18 and GmSANP11, compared to the wild-type soybean; and all of them were still resistant to SCN race 3 similar to the wild-type soybean.  Taken together, we can conclude that the 13 mutants identified in the present study carry the mutations of the new gene(s) which contribute(s) to the resistance to SCN race 4 in PI 437654 and can be potentially used as the genetic soybean sources to further identify the novel SCN-resistant gene(s).   
Keywords:  soybean        ethane methylsulfonate-mutagenesis populations        mutants       soybean cyst nematode race 4        resistance  
Received: 23 June 2018   Accepted:
Fund: This work was financially supported by the Innovation Program and Youth Elite Program of Chinese Academy of Agricultural Sciences and the Special Fund for Agro-scientific Research in the Public Interest of China (201503114).
Corresponding Authors:  Correspondence LIU Shi-ming, E-mail: smliuhn@yahoo.com   
About author:  Ge Feng-yong, E-mail: gefylc@163.com;

Cite this article: 

GE Feng-yong, ZHENG Na, ZHANG Liu-ping, HUANG Wen-kun, PENG De-liang, LIU Shi-ming. 2018. Chemical mutagenesis and soybean mutants potential for identification of novel genes conferring resistance to soybean cyst nematode. Journal of Integrative Agriculture, 17(12): 2734-2744.

Abe A, Kosugi S, Yoshida K, Natsume S, Takagi H, Kanzaki H, Matsumura H, Yoshida K, Mitsuoka C, Tamiru M, Innan H, Cano L, Kamoun S, Terauchi R. 2012. Genome sequencing reveals agronomically important loci in rice using MutMap. Nature Biotechnology, 30, 174–178.
Bayless A M, Smith J M, Song J, McMinn P H, Teillet A, August B K, Bent A F. 2016. Disease resistance through impairment of alpha-SNAP-NSF interaction and vesicular trafficking by soybean Rhg1. Proceedings of the National Academy of Sciences of the United States of America, 113, E7375–E7382.
Brown S, Yeckel G, Heinz R, Clark K, Sleper D, Mitchum M G. 2010. A high-throughput automated technique for counting females of Heterodera glycines using a fluorescence-based imaging system. Journal of Nematology, 42, 201–206.
Brucker E, Carlson S, Wright E, Niblack T, Diers B. 2005. Rhg1 alleles from soybean PI 437654 and PI 88788 respond differentially to isolates of Heterodera glycines in the greenhouse. Theoretical and Applied Genetics, 111, 44–49.
Cai Y, Chen L, Liu X, Guo C, Sun S, Wu C, Jiang B, Han T, Hou W. 2018. CRISPR/Cas9-mediated targeted mutagenesis of GmFT2a delays flowering time in soya bean. Plant Biotechnology Journal, 16, 176–185.
Colgrove A L, Niblack T L. 2008. Correlation of female indices from virulence assays on inbred lines and field populations of Heterodera glycines. Journal of Nematology, 40, 39–45.
Concibido V C, Diers B W, Arelli P R. 2004. A decade of QTL mapping for cyst nematode resistance in soybean. Crop Science, 44, 1121–1131.
Cook D E, Bayless A M, Wang K, Guo X, Song Q, Jiang J, Bent A F. 2014. Distinct copy number, coding sequence, and locus methylation patterns underlie Rhg1-mediated soybean resistance to soybean cyst nematode. Plant Physiology, 165, 630–647.
Cook D E, Lee T G, Guo X, Melito S, Wang K, Bayless A M, Wang J, Hughes T J, Willis D K, Clemente T E, Diers B W, Jiang J, Hudson M E, Bent A F. 2012. Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science, 338, 1206–1209.
Cooper J L, Till B J, Laport R G, Darlow M C, Kleffner J M, Jamai A, El-Mellouki T, Liu S, Ritchie R, Nielsen N, Bilyeu K D, Meksem K, Comai L, Henikoff S. 2008. TILLING to detect induced mutations in soybean. BMC Plant Biology, 8, 9.
Dalmais M, Schmidt J, Signor C L, Moussy F, Burstin J, Savois V, Aubert G, Brunaud V, Oliveira Y D, Guichard C, Thompson R, Bendahmane A. 2008. UTILLdb, a Pisum sativum in silico forward and reverse genetics tool. Genome Biology, 9, R43.
Dong C, Dalton-Morgan J, Vincent K, Sharp P. 2009. A modified TILLING method for wheat breeding. Plant Genome, 2, 39–47.
Greene E A, Codomo C A, Taylor N E, Henikoff J G, Till B J, Reynolds S H, Enns L C, Burtner C, Johnson J E, Odden A R, Comai L, Henikoff S. 2003. Spectrum of chemically induced mutations from a large-scale reverse-genetic screen in Arabidopsis. Genetics, 164, 731–740.
Kandoth P K, Heinz R, Yeckel G, Gross N W, Juvale P S, Hill J, Whitham S A, Baum T J, Mitchum M G. 2013. A virus-induced gene silencing method to study soybean cyst nematode parasitism in Glycine max. BMC Research Notes, 6, 255.
Kandoth P K, Liu S, Prenger E, Ludwig A, Lakhssassi N, Heinz R, Zhou Z, Howland A, Gunther J, Warren S, Dhroso A, Lafayette P, Tucker D, Johnson S, Anderson J, Alaswad A, Cianzio S R, Parrott W, Korkin D, Meksem K, et al. 2017. Systematic mutagenesis of serine hydroxymethyltransferase reveals an essential role in nematode resistance. Plant Physiology, 175, 1370–1380.
Koenning S R, Wrather J A. 2010. Suppression of soybean yield potential in the continental United States from plant diseases estimated from 2006 to 2009. Plant Health Progress, 11, 1.
Lakhssassi N, Liu S, Bekal S, Zhou Z, Colantonio V, Lambert K, Barakat A, Meksem K. 2017. Characterization of the soluble NSF attachment protein gene family identifies two members involved in additive resistance to a plant pathogen. Scientific Reports, 7, 45226.
Lee T G, Kumar I, Diers B W, Hudson M E. 2015. Evolution and selection of Rhg1, a copy-number variant nematode-resistance locus. Molecular Ecology, 24, 1774–1791.
Liu S, Kandoth P K, Lakhssassi N, Kang J, Colantonio V, Heinz R, Yechel G, Zhou Z, Bekal S, Dapprich J, Rotter B, Cianzio S, Mitchum M G, Meksem K. 2017. The soybean GmSNAP18 gene underlies two types of resistance to soybean cyst nematode. Nature Communications, 8, 14822.
Liu, S, Kandoth P K, Warren S D, Yechel G, Heinz R, Alden J, Yang C, Jamai A, Ei-Mellouki T, Juvale P S, Hill J, Baum T J, Cianzio S, Whitham S A, Korkin D, Mitchum M G, Meksem K. 2012. A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens. Nature, 492, 256–260.
Liu X, Liu A, Jami A, Bendahmane A, Lightfoot D A, Mitchum M G, Meksem K. 2011. Soybean cyst nematode resistance in soybean is independent of the Rhg4 locus LRR-RLK gene. Functional and Integrative Genomics, 11, 539–549.
McCallum C M, Comai L, Greene E A, Henikoff S. 2000. Targeted screening for induced mutations. Nature Biotechnology, 18, 455–457.
Meksem K, Liu S, Liu X, Jamai A, Mitchum M G, Bendahmane A, El-Mellouki T. 2008. TILLING: A reverse genetics and a functional genomics tool in soybean. In: Kahl G, Meksem K, eds., The Handbook of Plant Functional Genomics: Concepts and Protocols . WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany. pp. 251–265.
Meksem K, Pantazopoulos P, Njiti V N, Hyten L D, Arelli P R, Lightfoot D A. 2001. ‘Forrest’ resistance to the soybean cyst nematode is bigenic: Saturation mapping of the Rhg1 and Rhg4 loci. Theoretical and Applied Genetics, 103, 710–717.
Melito S, Heuberger A L, Cook D E, Diers B W, MacGuidwin A E, Bent A F. 2010. A nematode demographics assay in transgenic roots reveals no significant impacts of the Rhg1 locus LRR-Kinase on soybean cyst nematode resistance. BMC Plant Biology, 10, 104.
Mitchum M G. 2016. Soybean resistance to the soybean cyst nematode Heterodera glycines: An update. Phytopathology, 106, 1444–1450.
Mitchum M G, Wrather J A, Heinz R D, Shannon J G, Danekas G. 2007. Variability in distribution and virulence phenotypes of Heterodera glycines in Missouri during 2005. Plant Disease, 91, 1473–1476.
Niblack T L, Heinz R D, Smith G S, Donald P A. 1993. Distribution, density, and diversity of Heterodera glycines in Missouri. Journal of Nematology, 25, 880–886.
Peng D L, Pen H, Wu D Q, Huang W K, Ye W X, Cui J K. 2016. First report of soybean cyst nematode (Heterodera glycines) on soybean from Gansu and Ningxia China. Plant Disease, 100, 229.
Perry J A, Wang T L, Welham T J, Gardner S, Pike J M, Yoshida S, Parniske M. 2003. A TILLING reverse genetics tool and a web-accessible collection of mutants of the legume Lotus japonicus. Plant Physiology, 131, 866–871.
Porceddu A, Panara F, Calderini O, Molinari L, Taviani P, Lanfaloni L, Scotti C, Carelli M, Scaramelli L, Bruschi G, Cosson V, Ratet P, Larembergue H D, Duc G, Piano E, Arcioni S. 2008. An Italian functional genomic resource for Medicago truncatula. BMC Research Notes, 1, 129.
Schmutz J,  Cannon S B,  Schlueter J,  Ma J,  Mitros T,  Nelson W, Hyten D L,  Song Q,  Thelen J J,  Cheng J, Xu D, Hellsten U, May G D, Yu Y, Sakurai T, Umezawa T, Bhattacharyya M K, Sandhu D, Valliyodan B, Lindquist E, et al. 2010. Genome sequence of the palaeopolyploid soybean. Nature, 463, 178–183.
Shi Z, Liu S, Noe J, Arelli P, Meksem K, Li Z. 2015. SNP identification and marker assay development for high-throughput selection of soybean cyst nematode resistance. BMC Genomics, 16, 314.
Suzuki T, Eiguchi M, Kumamaru T, Satoh H, Matsusaka H, Moriguchi K, Nagato Y, Kurata N. 2008. MNU-induced mutant pools and high performance TILLING enable finding of any gene mutation in rice. Molecular Genetics and Genomics, 279, 213–223.
Takagi H, Abe A, Yoshida K, Kosugi S, Natsume S, Mitsuoka C, Uemura A, Utsushi H, Tamiru M, Takuno S, Innan H, Cano L M, Kamoun S, Terauchi R. 2013. QTL-seq: Rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. The Plant Journal, 74,174–183.
Takagi H, Tamiru M, Abe A, Yoshida K, Uemura A, Yaegashi H, Obara T, Oikawa K, Utsushi H, Kanzaki E, Mitsuoka C, Natsume S, Kosugi S, Kanzaki H, Matsumura H, Urasaki N, Kamoun S, Terauchi R. 2015. MutMap accelerates breeding of a salt-tolerant rice cultivar. Nature Biotechnology, 33, 445–449.
Talamè V, Bovina R, Sanguineti M C, Tuberosa R, Lundqvist U, Salvi S. 2008. TILLMore, a resource for the discovery of chemically induced mutants in barley. Plant Biotechnology Journal, 6, 477–485.
Till B J, Reynolds S H, Weil C, Springer N, Burtner C, Young K, Bowers E, Codomo C A, Enns L C, Odden A R, Greene E A, Comai L, Henikoff S. 2004. Discovery of induced point mutations in maize genes by TILLING. BMC Plant Biology, 4, 12.
Wang N, Wang Y, Tian F, King G J, Zhang C, Long Y, Shi L, Meng J. 2008. A functional genomics resource for Brassica napus: Development of an EMS mutagenized population and discovery of FAE1 point mutations by TILLING. New Phytologist, 180, 751–765.
Wu X, Blake S, Sleper D A, Shannon J G, Cregan P, Nguyen H T. 2009. QTL, additive and epistatic effects for SCN resistance in PI 437654. Theoretical and Applied Genetics, 118, 1093–1105.
Yu N, Lee T G, Rosa D P, Hudson M, Diers B W. 2016. Impact of Rhg1 copy number, type, and interaction with Rhg4 on resistance to Heterodera glycines in soybean. Theoretical and Applied Genetics, 129, 2403–2412.
Xin Z, Wang M L, Barkley N A, Burow G, Franks C, Pederson G, Burke J. 2008. Applying genotyping (TILLING) and phenotyping analyses to elucidate gene function in a chemically induced sorghum mutant population. BMC Plant Biology, 8, 103.
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