Genetic variation and genetic complexity of nodule occupancy in soybean inoculated with USDA110 and USDA123 rhizobium strains

Araya, Susan; Elia, Patrick; Quigley, Charles V.; Song, Qijian

doi:10.1186/s12864-023-09627-4

Title: Genetic variation and genetic complexity of nodule occupancy in soybean inoculated with USDA110 and USDA123 rhizobium strains

Journal Article · 04 September 2023 · BMC Genomics

DOI: https://doi.org/10.1186/s12864-023-09627-4 · OSTI ID:1998020

Araya, Susan; Elia, Patrick; Quigley, Charles V.;

Abstract Background Symbiotic nitrogen fixation differs among Bradyrhizobium japonicum strains. Soybean inoculated with USDA123 has a lower yield than strains known to have high nitrogen fixation efficiency, such as USDA110. In the main soybean-producing area in the Midwest of the United States, USDA123 has a high nodule incidence in field-grown soybean and is competitive but inefficient in nitrogen fixation. In this study, a high-throughput system was developed to characterize nodule number among 1,321 Glycine max and 69 Glycine soja accessions single inoculated with USDA110 and USDA123. Results Seventy-three G. max accessions with significantly different nodule number of USDA110 and USDA123 were identified. After double inoculating 35 of the 73 accessions, it was observed that PI189939, PI317335, PI324187B, PI548461, PI562373, and PI628961 were occupied by USDA110 and double-strain nodules but not by USDA123 nodules alone. PI567624 was only occupied by USDA110 nodules, and PI507429 restricted all strains. Analysis showed that 35 loci were associated with nodule number in G. max when inoculated with strain USDA110 and 35 loci with USDA123. Twenty-three loci were identified in G. soja when inoculated with strain USDA110 and 34 with USDA123. Only four loci were common across two treatments, and each locus could only explain 0.8 to 1.5% of phenotypic variation. Conclusions High-throughput phenotyping systems to characterize nodule number and occupancy were developed, and soybean germplasm restricting rhizobium strain USDA123 but preferring USDA110 was identified. The larger number of minor effects and a small few common loci controlling the nodule number indicated trait genetic complexity and strain-dependent nodulation restriction. The information from the present study will add to the development of cultivars that limit USDA123, thereby increasing nitrogen fixation efficiency and productivity.

View Journal Article

Cite

Export

Save

Sponsoring Organization:: USDOE

OSTI ID:: 1998020

Journal Information:: BMC Genomics, Journal Name: BMC Genomics Journal Issue: 1 Vol. 24; ISSN 1471-2164

Publisher:: Springer Science + Business MediaCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (72)

Field release of genetically-engineered Rhizobium meliloti and Bradyrhizobium japonicum strains Ronson, C. W.; Bosworth, A.; Genova, M. Nitrogen Fixation https://doi.org/10.1007/978-1-4684-6432-0_41	book	January 1990
A single dominant gene in McCall soybean prevents effective nodulation with Rhizobium fredii USDA257 Trese, Arthur T. Euphytica, Vol. 81, Issue 3 https://doi.org/10.1007/BF00025618	journal	January 1995
Occurrence and nature of mixed infections in nodules of field-grown soybeans (Glycine max) Moawad, M.; Schmidt, E. L. Biology and Fertility of Soils, Vol. 5, Issue 2 https://doi.org/10.1007/BF00257644	journal	November 1987
Regulation of nod gene expression in Bradyrhizobium japonicum Banfalvi, Zsofia; Nieuwkoop, Anthony; Schell, Maria Molecular and General Genetics MGG, Vol. 214, Issue 3 https://doi.org/10.1007/BF00330475	journal	November 1988
Cultivar and pH effects on competition for nodule sites between isolates of Rhizobium in beans Vargas, Alvaro A. T.; Graham, Peter H. Plant and Soil, Vol. 117, Issue 2 https://doi.org/10.1007/BF02220712	journal	July 1989
Diverse bacteria isolated from root nodules of Trifolium, Crotalaria and Mimosa grown in the subtropical regions of China Liu, Xiao Yun; Wang, En Tao; Li, Ying Archives of Microbiology, Vol. 188, Issue 1 https://doi.org/10.1007/s00203-007-0209-x	journal	May 2007
Retrieved 16S rRNA and nifH sequences reveal co-dominance of Bradyrhizobium and Ensifer (Sinorhizobium) strains in field-collected root nodules of the promiscuous host Vigna radiata (L.) R. Wilczek Hakim, Sughra; Mirza, Babur S.; Zaheer, Ahmad Applied Microbiology and Biotechnology, Vol. 102, Issue 1 https://doi.org/10.1007/s00253-017-8609-6	journal	November 2017
Can introduced and indigenous rhizobial strains compete for nodule formation by promiscuous soybean in the moist savanna agroecological zone of Nigeria? Sanginga, N.; Okogun, J. A. Biology and Fertility of Soils, Vol. 38, Issue 1 https://doi.org/10.1007/s00374-003-0611-8	journal	June 2003
Biodiversity of endophytic bacteria which colonize red clover nodules, roots, stems and foliage and their influence on host growth Sturz, A. V.; Christie, B. R.; Matheson, B. G. Biology and Fertility of Soils, Vol. 25, Issue 1 https://doi.org/10.1007/s003740050273	journal	May 1997
QTL analysis of nodule traits and the identification of loci interacting with the type III secretion system in soybean Zhu, Jingyi; Wang, Jinhui; Li, Qingying Molecular Genetics and Genomics, Vol. 294, Issue 4 https://doi.org/10.1007/s00438-019-01553-z	journal	April 2019
Genetics and mapping of quantitative traits for nodule number, weight, and size in soybean (Glycine max L.[Merr.]) Hwang, Sadal; Ray, Jeffery D.; Cregan, Perry B. Euphytica, Vol. 195, Issue 3 https://doi.org/10.1007/s10681-013-1005-0	journal	October 2013
Diverse bacterial taxa inhabit root nodules of lucerne (Medicago sativa L.) in New Zealand pastoral soils Wigley, Kathryn; Moot, Derrick; Wakelin, Steve A. Plant and Soil, Vol. 420, Issue 1-2 https://doi.org/10.1007/s11104-017-3395-6	journal	August 2017
Identification of quantitative trait loci controlling nodulation and shoot mass in progenies from two Brazilian soybean cultivars Nicolás, Marisa F.; Hungria, Mariangela; Arias, Carlos A. A. Field Crops Research, Vol. 95, Issue 2-3 https://doi.org/10.1016/j.fcr.2005.04.012	journal	February 2006
Soybean cultivars affect nodulation competition of Bradyrhizobium japonicum strains Payakapong, Waraporn; Tittabutr, Panlada; Teaumroong, Neung World Journal of Microbiology and Biotechnology, Vol. 20, Issue 3 https://doi.org/10.1023/B:WIBI.0000023838.06663.c5	journal	January 2004
Induction of Bradyrhizobium japonicum common nod genes by isoflavones isolated from Glycine max Kosslak, Renee M.; Bookland, Roger; Barkei, John Proceedings of the National Academy of Sciences, Vol. 84, Issue 21 https://doi.org/10.1073/pnas.84.21.7428	journal	November 1987
Haploview: analysis and visualization of LD and haplotype maps Barrett, J. C.; Fry, B.; Maller, J. Bioinformatics, Vol. 21, Issue 2 https://doi.org/10.1093/bioinformatics/bth457	journal	August 2004
TASSEL: software for association mapping of complex traits in diverse samples Bradbury, P. J.; Zhang, Z.; Kroon, D. E. Bioinformatics, Vol. 23, Issue 19 https://doi.org/10.1093/bioinformatics/btm308	journal	June 2007
Phytozome: a comparative platform for green plant genomics Goodstein, David M.; Shu, Shengqiang; Howson, Russell Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr944	journal	November 2011
agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update Tian, Tian; Liu, Yue; Yan, Hengyu Nucleic Acids Research, Vol. 45, Issue W1 https://doi.org/10.1093/nar/gkx382	journal	May 2017
A Thaumatin-Like Protein, Rj4, Controls Nodule Symbiotic Specificity in Soybean Hayashi, Masaki; Shiro, Sokichi; Kanamori, Hiroyuki Plant and Cell Physiology, Vol. 55, Issue 9 https://doi.org/10.1093/pcp/pcu099	journal	July 2014
Development and Application of a Multilocus Sequence Analysis Method for the Identification of Genotypes Within Genus Bradyrhizobium and for Establishing Nodule Occupancy of Soybean (Glycine max L. Merr) van Berkum, Peter; Elia, Patrick; Song, Qijian Molecular Plant-Microbe Interactions®, Vol. 25, Issue 3 https://doi.org/10.1094/MPMI-09-11-0241	journal	March 2012
Rhizobium tropici Genes Involved in Free-Living Salt Tolerance are Required for the Establishment of Efficient Nitrogen-Fixing Symbiosis with Phaseolus vulgaris Nogales, Joaquina; Campos, Rosario; BenAbdelkhalek, Hanaa Molecular Plant-Microbe Interactions, Vol. 15, Issue 3 https://doi.org/10.1094/MPMI.2002.15.3.225	journal	March 2002
Effects of Spore Density and Interaction With Heterodera glycines on Soybean Root Rot Caused by Fusarium solani and F. tricinctum Yan, Hui; Nelson, Berlin Plant Disease, Vol. 105, Issue 9 https://doi.org/10.1094/PDIS-09-20-1944-RE	journal	September 2021
Assessing Direct and Residual Effects of Cover Crops on the Soybean Cyst Nematode, Heterodera glycines Harbach, Chelsea J.; Tylka, Gregory L. Plant Disease, Vol. 106, Issue 5 https://doi.org/10.1094/PDIS-12-20-2581-RE	journal	May 2022
Evidence for Double Infection Within Soybean Nodules Lindemann, W. C.; Schmidt, E. L.; Ham, G. E. Soil Science, Vol. 118, Issue 4 https://doi.org/10.1097/00010694-197410000-00009	journal	October 1974
Fast model-based estimation of ancestry in unrelated individuals Alexander, D. H.; Novembre, J.; Lange, K. Genome Research, Vol. 19, Issue 9 https://doi.org/10.1101/gr.094052.109	journal	July 2009
sym 13—A Gene Conditioning Ineffective Nodulation in Pisum sativum Kneen, Barbara E.; LaRue, Thomas A.; Hirsch, Ann M. Plant Physiology, Vol. 94, Issue 3 https://doi.org/10.1104/pp.94.3.899	journal	November 1990
Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue Cooper, J. E. Journal of Applied Microbiology, Vol. 103, Issue 5 https://doi.org/10.1111/j.1365-2672.2007.03366.x	journal	April 2007
PCR inhibitors - occurrence, properties and removal Schrader, C.; Schielke, A.; Ellerbroek, L. Journal of Applied Microbiology, Vol. 113, Issue 5 https://doi.org/10.1111/j.1365-2672.2012.05384.x	journal	July 2012
Relative genetic structure of a population of Rhizobium meliloti isolated directly from soil and from nodules of alfalfa (Medicago sativa) and sweet clover (Melilotus alba) Bromfield, E. S. P.; Barran, L. R.; Wheatcroft, R. Molecular Ecology, Vol. 4, Issue 2 https://doi.org/10.1111/j.1365-294X.1995.tb00207.x	journal	April 1995
Endogenous isoflavones are essential for the establishment of symbiosis between soybean andBradyrhizobium japonicum Subramanian, Senthil; Stacey, Gary; Yu, Oliver The Plant Journal, Vol. 48, Issue 2 https://doi.org/10.1111/j.1365-313X.2006.02874.x	journal	October 2006
Mapping of QTLs associated with biological nitrogen fixation traits in soybean Santos, Maria Aparecida; Geraldi, Isaias Olívio; Garcia, Antonio Augusto Franco Hereditas, Vol. 150, Issue 2-3 https://doi.org/10.1111/j.1601-5223.2013.02275.x	journal	June 2013
Studies on double strain occupancy of nodules and the competitive ability of Rhizobium trifolii on red and white clover grown in soil and agar Bromfield, E. S. P.; Jones, D. Gareth Annals of Applied Biology, Vol. 94, Issue 1 https://doi.org/10.1111/j.1744-7348.1980.tb03895.x	journal	January 1980
Two cultivated legume plants reveal the enrichment process of the microbiome in the rhizocompartments Xiao, Xiao; Chen, Weimin; Zong, Le Molecular Ecology, Vol. 26, Issue 6 https://doi.org/10.1111/mec.14027	journal	February 2017
A VIT‐like transporter facilitates iron transport into nodule symbiosomes for nitrogen fixation in soybean Liu, Sheng; Liao, Li Li; Nie, Miao Miao New Phytologist, Vol. 226, Issue 5 https://doi.org/10.1111/nph.16506	journal	March 2020
GmVTL1a is an iron transporter on the symbiosome membrane of soybean with an important role in nitrogen fixation Brear, Ella M.; Bedon, Frank; Gavrin, Aleksandr New Phytologist, Vol. 228, Issue 2 https://doi.org/10.1111/nph.16734	journal	July 2020
The Medicago truncatula Vacuolar iron Transporter‐Like proteins VTL4 and VTL8 deliver iron to symbiotic bacteria at different stages of the infection process Walton, Jennifer H.; Kontra‐Kováts, Gyöngyi; Green, Robert T. New Phytologist, Vol. 228, Issue 2 https://doi.org/10.1111/nph.16735	journal	July 2020
Functional analysis of alternative transcripts of the soybean Rj2 gene that restricts nodulation with specific rhizobial strains Tang, F.; Yang, S.; Zhu, H. Plant Biology, Vol. 18, Issue 3 https://doi.org/10.1111/plb.12442	journal	February 2016
Mutant Strains of Rhizobium japonicum with Increased Ability to Fix Nitrogen for Soybean Maier, Robert J.; Brill, Winston J. Science, Vol. 201, Issue 4354 https://doi.org/10.1126/science.201.4354.448	journal	August 1978
Photosynthetic Bradyrhizobium sp. Strain ORS285 Is Capable of Forming Nitrogen-Fixing Root Nodules on Soybeans (Glycine max) Giraud, Eric; Xu, Lei; Chaintreuil, Clï¿½mence Applied and Environmental Microbiology, Vol. 79, Issue 7 https://doi.org/10.1128/AEM.03735-12	journal	April 2013
Rhizosphere Response as a Factor in Competition Among Three Serogroups of Indigenous Rhizobium japonicum for Nodulation of Field-Grown Soybeans Moawad, H. A.; Ellis, W. R.; Schmidt, E. L. Applied and Environmental Microbiology, Vol. 47, Issue 4 https://doi.org/10.1128/aem.47.4.607-612.1984	journal	April 1984
Nodulation and Competition for Nodulation of Selected Soybean Genotypes among Bradyrhizobium japonicum Serogroup 123 Isolates Keyser, H. H.; Cregan, P. B. Applied and Environmental Microbiology, Vol. 53, Issue 11 https://doi.org/10.1128/aem.53.11.2631-2635.1987	journal	November 1987
Influence of Glycine spp. on Competitiveness of Bradyrhizobium japonicum and Rhizobium fredii Cregan, P. B.; Keyser, H. H. Applied and Environmental Microbiology, Vol. 54, Issue 3 https://doi.org/10.1128/aem.54.3.803-808.1988	journal	March 1988
Improvement of Rhizobium Inoculants Paau, Alan S. Applied and Environmental Microbiology, Vol. 55, Issue 4 https://doi.org/10.1128/aem.55.4.862-865.1989	journal	April 1989
DNA Hybridization Probe for Use in Determining Restricted Nodulation among Bradyrhizobium japonicum Serocluster 123 Field Isolates Sadowsky, Michael J.; Cregan, Perry B.; Keyser, Harold H. Applied and Environmental Microbiology, Vol. 56, Issue 6 https://doi.org/10.1128/aem.56.6.1768-1774.1990	journal	June 1990
The Soybean Rj4 Allele Restricts Nodulation by Bradyrhizobium japonicum Serogroup 123 Strains Sadowsky, Michael J.; Cregan, Perry B. Applied and Environmental Microbiology, Vol. 58, Issue 2 https://doi.org/10.1128/aem.58.2.720-723.1992	journal	February 1992
Host-Controlled Restriction of Nodulation by Bradyrhizobium japonicum Strains in Serogroup 110 Lohrke, S. M.; Orf, J. H.; Martinez-Romero, E. Applied and Environmental Microbiology, Vol. 61, Issue 6 https://doi.org/10.1128/aem.61.6.2378-2383.1995	journal	June 1995
A Simple Assembly for Use in the Testing of Cultures of Rhizobia Leonard, Lewis T. Journal of Bacteriology, Vol. 45, Issue 6 https://doi.org/10.1128/jb.45.6.523-527.1943	journal	June 1943
A genome-wide association study of seed protein and oil content in soybean Hwang, Eun-Young; Song, Qijian; Jia, Gaofeng BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-1	journal	January 2014
WASP: a Web-based Allele-Specific PCR assay designing tool for detecting SNPs and mutations Wangkumhang, Pongsakorn; Chaichoompu, Kridsadakorn; Ngamphiw, Chumpol BMC Genomics, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2164-8-275	journal	August 2007
Construction of high resolution genetic linkage maps to improve the soybean genome sequence assembly Glyma1.01 Song, Qijian; Jenkins, Jerry; Jia, Gaofeng BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-015-2344-0	journal	January 2016
High throughput DNA extraction of legume root nodules for rhizobial metagenomics Johnson, Gabriel AMB Express, Vol. 9, Issue 1 https://doi.org/10.1186/s13568-019-0771-z	journal	April 2019
High-quality permanent draft genome sequence of the Bradyrhizobium elkanii type strain USDA 76T, isolated from Glycine max (L.) Merr Reeve, Wayne; van Berkum, Peter; Ardley, Julie Standards in Genomic Sciences, Vol. 12, Issue 1 https://doi.org/10.1186/s40793-017-0238-2	journal	March 2017
Rj (rj) genes involved in nitrogen-fixing root nodule formation in soybean Hayashi, Masaki; Saeki, Yuichi; Haga, Michiyo Breeding Science, Vol. 61, Issue 5 https://doi.org/10.1270/jsbbs.61.544	journal	January 2012
Serogroups of Rhizobium japonicum in Soybean Nodules as Affected by Soil Types¹ Damirgi, S. M.; Frederick, L. R.; Anderson, I. C. Agronomy Journal, Vol. 59, Issue 1 https://doi.org/10.2134/agronj1967.00021962005900010004x	journal	January 1967
Serogroups of Rhizobium japonicum in Soybean Nodules Sampled in Iowa¹ Ham, G. E.; Frederick, L. R.; Anderson, I. C. Agronomy Journal, Vol. 63, Issue 1 https://doi.org/10.2134/agronj1971.00021962006300010022x	journal	January 1971
Evaluation of Rhizobium japonicum Inoculants in Soils Containing Naturalized Populations of Rhizobia¹ Ham, G. E.; Cardwell, V. B.; Johnson, H. W. Agronomy Journal, Vol. 63, Issue 2 https://doi.org/10.2134/agronj1971.00021962006300020030x	journal	March 1971
Influence of Inoculum Size on Rhizobium japonicum Serogroup Distribution Frequency in Soybean Nodules¹ Kapusta, George; Rouwenhorst, D. L. Agronomy Journal, Vol. 65, Issue 6 https://doi.org/10.2134/agronj1973.00021962006500060021x	journal	November 1973
Effect of Inoculum Rate on Competitive Nodulation of Glycine max L. Merrill. II. Field Studies¹ Weaver, R. W.; Frederick, L. R. Agronomy Journal, Vol. 66, Issue 2 https://doi.org/10.2134/agronj1974.00021962006600020015x	journal	March 1974
Evaluation of Peat and Granular Inoculum for Soybean Yield and N Fixation Under Irrigation¹ Bezdicek, D. F.; Evans, D. W.; Abede, Evans B. Agronomy Journal, Vol. 70, Issue 5 https://doi.org/10.2134/agronj1978.00021962007000050037x	journal	September 1978
Recovery of Introduced Rhizobium japonicum Strains by Soybean Genotypes¹ Kvien, C. S.; Ham, G. E.; Lambert, J. W. Agronomy Journal, Vol. 73, Issue 5 https://doi.org/10.2134/agronj1981.00021962007300050034x	journal	September 1981
Introduction and Survival of an Inoculant Strain of Rhizobium japonicumin Soil¹ Dunigan, E. P.; Bollich, P. K.; Hutchinson, R. L. Agronomy Journal, Vol. 76, Issue 3 https://doi.org/10.2134/agronj1984.00021962007600030023x	journal	May 1984
Persistence and Recovery of Rhizobium japonicum Inoculum in a Field Soil ¹ Ellis, W. R.; Ham, G. E.; Schmidt, E. L. Agronomy Journal, Vol. 76, Issue 4 https://doi.org/10.2134/agronj1984.00021962007600040015x	journal	July 1984
Serological Distribution of Bradyrhizobium japonicum from U.S. Soybean Production Areas Weber, D. F.; Keyser, H. H.; Uratsu, S. L. Agronomy Journal, Vol. 81, Issue 5 https://doi.org/10.2134/agronj1989.00021962008100050018x	journal	September 1989
Inheritance of a Strain‐Specific Ineffective Nodulation in Soybeans ¹ Caldwell, B. E. Crop Science, Vol. 6, Issue 5 https://doi.org/10.2135/cropsci1966.0011183X000600050010x	journal	September 1966
Effects of Rhizobium japonicum Strains on Soybean Yields ¹ Caldwell, B. E.; Vest, Grant Crop Science, Vol. 10, Issue 1 https://doi.org/10.2135/cropsci1970.0011183X001000010008x	journal	January 1970
Rj ₄ — A Gene Conditioning Ineffective Nodulation in Soybean ¹ Vest, Grant; Caldwell, B. E. Crop Science, Vol. 12, Issue 5 https://doi.org/10.2135/cropsci1972.0011183X001200050042x	journal	September 1972
Nitrogen Fixation by Soybeans: Seasonal and Cultivar Effects, and Comparison of Estimates ¹ Patterson, T. G.; LaRue, T. A. Crop Science, Vol. 23, Issue 3 https://doi.org/10.2135/cropsci1983.0011183X002300030012x	journal	May 1983
Host Restriction of Nodulation by Bradyrhizobium japonicum Strain USDA 123 in Soybean ¹ Cregan, P. B.; Keyser, H. H. Crop Science, Vol. 26, Issue 5 https://doi.org/10.2135/cropsci1986.0011183X002600050016x	journal	September 1986
Soybean Genotype Restricting Nodulation of a Previously Unrestricted Serocluster 123 Bradyrhizobia Cregan, P. B.; Keyser, H. H.; Sadowsky, M. J. Crop Science, Vol. 29, Issue 2 https://doi.org/10.2135/cropsci1989.0011183X002900020015x	journal	January 1989
Soybean Nitrogen Fixation and Nitrogen Remobilization during Reproductive Development Mastrodomenico, Adriano T.; Purcell, Larry C. Crop Science, Vol. 52, Issue 3 https://doi.org/10.2135/cropsci2011.08.0414	journal	May 2012
Selenium hyperaccumulation by Astragalus (Fabaceae) does not inhibit root nodule symbiosis Alford, Élan R.; Pilon-Smits, Elizabeth A. H.; Fakra, Sirine C. American Journal of Botany, Vol. 99, Issue 12 https://doi.org/10.3732/ajb.1200124	journal	December 2012

Similar Records

Construction and comparison of three reference-quality genome assemblies for soybean

Journal Article · 2019 · The Plant Journal · OSTI ID:1619141

Valliyodan, Babu; Cannon, Steven B.; Bayer, Philipp E.; +27 more

Ureide assay for measuring nitrogen fixation by nodulated soybean calibrated by sup 15 N methods. [Glycine max]

Journal Article · 1990 · Plant Physiology; (USA) · OSTI ID:5941429

Herridge, D F; Peoples, M B

Measurement of nitrogen fixation by soybean in the field using the ureide and natural sup 15 N abundance methods. [Glycine max (L. )]

Journal Article · 1990 · Plant Physiology; (USA) · OSTI ID:5852778

Herridge, D F; Bergersen, F J; Peoples, M B

Title: Genetic variation and genetic complexity of nodule occupancy in soybean inoculated with USDA110 and USDA123 rhizobium strains

Citation Formats

References (72)

Similar Records

Related Subjects