Identification of loci associated with water use efficiency and symbiotic nitrogen fixation in soybean

Identification of loci associated with water use efficiency and symbiotic nitrogen fixation in soybean

Soybean ( Glycine max ) production is greatly affected by persistent and/or intermittent droughts in rainfed soybean-growing regions worldwide. Symbiotic N 2 fixation (SNF) in soybean can also be significantly hampered even under moderate drought stress. The objective of this study was to identify g...

Full description

Saved in:
Bibliographic Details
Published in:Frontiers in plant science Vol. 14; p. 1271849
Main Authors: Arifuzzaman, Muhammad, Mamidi, Sujan, Sanz-Saez, Alvaro, Zakeri, Hossein, Scaboo, Andrew, Fritschi, Felix B.
Format: Journal Article
Language:English
Published: Frontiers Media S.A 16-11-2023
Subjects:
carbon isotope ratio
genome-wide association mapping
nitrogen isotope ratio
Plant Science
water use efficiency
whole genome resequencing
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
Abstract Soybean ( Glycine max ) production is greatly affected by persistent and/or intermittent droughts in rainfed soybean-growing regions worldwide. Symbiotic N 2 fixation (SNF) in soybean can also be significantly hampered even under moderate drought stress. The objective of this study was to identify genomic regions associated with shoot carbon isotope ratio (δ 13 C) as a surrogate measure for water use efficiency (WUE), nitrogen isotope ratio (δ 15 N) to assess relative SNF, N concentration ([N]), and carbon/nitrogen ratio (C/N). Genome-wide association mapping was performed with 105 genotypes and approximately 4 million single-nucleotide polymorphism markers derived from whole-genome resequencing information. A total of 11, 21, 22, and 22 genomic loci associated with δ 13 C, δ 15 N, [N], and C/N, respectively, were identified in two environments. Nine of these 76 loci were stable across environments, as they were detected in both environments. In addition to the 62 novel loci identified, 14 loci aligned with previously reported quantitative trait loci for different C and N traits related to drought, WUE, and N 2 fixation in soybean. A total of 58 Glyma gene models encoding for different genes related to the four traits were identified in the vicinity of the genomic loci.
AbstractList Soybean (Glycine max) production is greatly affected by persistent and/or intermittent droughts in rainfed soybean-growing regions worldwide. Symbiotic N2 fixation (SNF) in soybean can also be significantly hampered even under moderate drought stress. The objective of this study was to identify genomic regions associated with shoot carbon isotope ratio (δ13C) as a surrogate measure for water use efficiency (WUE), nitrogen isotope ratio (δ15N) to assess relative SNF, N concentration ([N]), and carbon/nitrogen ratio (C/N). Genome-wide association mapping was performed with 105 genotypes and approximately 4 million single-nucleotide polymorphism markers derived from whole-genome resequencing information. A total of 11, 21, 22, and 22 genomic loci associated with δ13C, δ15N, [N], and C/N, respectively, were identified in two environments. Nine of these 76 loci were stable across environments, as they were detected in both environments. In addition to the 62 novel loci identified, 14 loci aligned with previously reported quantitative trait loci for different C and N traits related to drought, WUE, and N2 fixation in soybean. A total of 58 Glyma gene models encoding for different genes related to the four traits were identified in the vicinity of the genomic loci.
Soybean ( Glycine max ) production is greatly affected by persistent and/or intermittent droughts in rainfed soybean-growing regions worldwide. Symbiotic N 2 fixation (SNF) in soybean can also be significantly hampered even under moderate drought stress. The objective of this study was to identify genomic regions associated with shoot carbon isotope ratio (δ 13 C) as a surrogate measure for water use efficiency (WUE), nitrogen isotope ratio (δ 15 N) to assess relative SNF, N concentration ([N]), and carbon/nitrogen ratio (C/N). Genome-wide association mapping was performed with 105 genotypes and approximately 4 million single-nucleotide polymorphism markers derived from whole-genome resequencing information. A total of 11, 21, 22, and 22 genomic loci associated with δ 13 C, δ 15 N, [N], and C/N, respectively, were identified in two environments. Nine of these 76 loci were stable across environments, as they were detected in both environments. In addition to the 62 novel loci identified, 14 loci aligned with previously reported quantitative trait loci for different C and N traits related to drought, WUE, and N 2 fixation in soybean. A total of 58 Glyma gene models encoding for different genes related to the four traits were identified in the vicinity of the genomic loci.
Author Mamidi, Sujan
Fritschi, Felix B.
Sanz-Saez, Alvaro
Arifuzzaman, Muhammad
Zakeri, Hossein
Scaboo, Andrew
AuthorAffiliation 1 Division of Plant Science and Technology, University of Missouri , Columbia, MO , United States
2 HudsonAlpha Institute for Biotechnology , Huntsville, AL , United States
4 College of Agriculture, California State University-Chico , Chico, CA , United States
3 Department of Crop, Soil and Environmental Sciences, Auburn University , Auburn, AL , United States
AuthorAffiliation_xml – name: 2 HudsonAlpha Institute for Biotechnology , Huntsville, AL , United States
– name: 3 Department of Crop, Soil and Environmental Sciences, Auburn University , Auburn, AL , United States
– name: 4 College of Agriculture, California State University-Chico , Chico, CA , United States
– name: 1 Division of Plant Science and Technology, University of Missouri , Columbia, MO , United States
Author_xml – sequence: 1
  givenname: Muhammad
  surname: Arifuzzaman
  fullname: Arifuzzaman, Muhammad
– sequence: 2
  givenname: Sujan
  surname: Mamidi
  fullname: Mamidi, Sujan
– sequence: 3
  givenname: Alvaro
  surname: Sanz-Saez
  fullname: Sanz-Saez, Alvaro
– sequence: 4
  givenname: Hossein
  surname: Zakeri
  fullname: Zakeri, Hossein
– sequence: 5
  givenname: Andrew
  surname: Scaboo
  fullname: Scaboo, Andrew
– sequence: 6
  givenname: Felix B.
  surname: Fritschi
  fullname: Fritschi, Felix B.
BookMark eNpVkU1rGzEQhpeSQJM0PyA3HXuxq-_VnkoJTWoI5JJCb2JWGjkKa8mV1k397yvXpjRzmWHm5Zlh3svuLOWEXXfD6FIIM3wK26kuOeViyXjPjBzedRdMa7mQmv84-69-313X-kJbKEqHob_owspjmmOIDuaYE8mBTNlFArW2BDN68hrnZ_LaykJ2FQmGJo6Y3J5A8qTuN2PMc3QkxbnkNSYS4u8jLCZS835ESB-68wBTxetTvuq-3319uv22eHi8X91-eVg4Mah5oXQY3QiCKWmoGHvOvZGgmVfKGwgGNQyGStMryVF49H0ABBFYj0orZ8RVtzpyfYYXuy1xA2VvM0T7t5HL2kJpx05oQY-hd9p7rqkMejQamEMTRg3g25rG-nxkbXfjBr1rfyowvYG-naT4bNf5l2VUm15K1QgfT4SSf-6wznYTq8NpgoR5Vy03gza0p5o2KTtKXcm1Fgz_9jBqDybbg8n2YLI9mSz-ALuHoPw
Cites_doi 10.1371/journal.pone.0101218
10.1104/PP.125.1.61
10.3835/plantgenome2016.02.0012
10.1093/jxb/erh100
10.1080/10256010500230106
10.4161/FLY.19695
10.2135/CROPSCI2017.07.0439
10.2135/CROPSCI1990.0011183X003000020011X
10.3389/FPLS.2019.00314/BIBTEX
10.1534/G3.115.021774
10.1023/A:1004289609466
10.2135/CROPSCI2013.09.0618
10.2136/SSSAJ1979.03615995004300060014X
10.1007/S00122-010-1292-Y/FIGURES/5
10.1007/s11120-013-9891-5
10.1093/bioinformatics/btz308
10.1038/303685a0
10.2135/cropsci2019.02.0085
10.3389/FPLS.2019.00075/BIBTEX
10.1093/AOB/MCU029
10.1016/j.ajhg.2013.10.026
10.1038/s41598-020-62034-7
10.1038/nrg.2016.49
10.1111/PPL.13201
10.2135/CROPSCI2016.05.0348
10.2135/CROPSCI2001.412493X
10.1016/J.PLAPHY.2021.09.026
10.3390/AGRONOMY12040946/S1
10.3390/IJMS20133137
10.3389/FPLS.2018.01690/BIBTEX
10.3389/FPLS.2020.00009/BIBTEX
10.1016/j.tcb.2004.07.016
10.2135/CROPSCI2001.4141099X
10.1186/s12864-019-6170-7
10.1111/J.1601-5223.2013.02275.X
10.1002/9780470650202.ch2
10.1038/ncomms15452
10.1016/S1369-5266(00)00168-0
10.1038/s41598-019-41922-7
10.1002/csc2.20240
10.1007/s11033-021-07030-4
10.2134/AGRONJ2009.0195
10.2135/CROPSCI2000.4061803X
10.1007/S00425-005-0020-3
10.1093/JXB/ERT369
10.1016/B978-044450965-9/50013-6
10.3389/fpls.2021.679463
10.2135/cropsci2002.1220
10.1104/PP.104.056317
10.1007/S11032-020-01140-W/FIGURES/2
10.1371/journal.pgen.1005767
10.1086/519795
10.1016/j.fcr.2016.03.001
10.1111/J.1399-3054.1996.TB05708.X
10.3835/plantgenome2014.11.0086
10.3389/FPLS.2020.00062/BIBTEX
10.1016/0031-9422(81)85134-5
10.3390/ijms20102422
10.1146/annurev.pp.40.060189.002443
10.1007/s00122-008-0825-0
10.1371/journal.pone.0125174
10.2135/cropsci1991.0011183x003100060046x
10.1007/s00122-014-2413-9
10.1007/s10681-020-02726-3
10.2135/cropsci2004.4840
10.1007/BF00011896
10.1371/journal.pone.0107469
10.1007/S10681-007-9449-8/FIGURES/4
10.3389/fpls.2016.01015
10.1016/0038-0717(95)98645-5
10.3389/fpls.2018.00610
10.2134/agronj1987.00021962007900060007x
10.1007/s10681-017-1966-5
10.1093/JXB/ERT332
10.1038/nature05491
10.1186/s40064-016-3019-2
10.1371/JOURNAL.PONE.0054985
10.3389/FPLS.2015.01223/BIBTEX
10.2135/CROPSCI1989.0011183X002900010023X
10.1007/s00438-019-01563-x
10.1126/science.1257800
10.1093/jxb/38.2.311
10.1016/J.PLANTSCI.2021.111007
10.3198/jpr2007.01.0046crg
10.1186/s12859-016-1227-y
10.2134/AGRONJ1991.00021962008300020011X
10.1016/0929-1393(95)00052-M
10.1371/journal.pone.0108179
10.3390/PLANTS12051004/S1
10.1007/s00122-020-03586-0
10.2135/CROPSCI2002.1110
10.1016/J.FCR.2017.08.009
10.1214/SS/1177011926
10.1007/BF02149646/METRICS
10.1038/srep28225
10.2135/cropsci2006.03.0165
10.1016/J.MOLP.2017.10.001
10.2135/CROPSCI1997.0011183X003700050011X
10.1146/annurev-arplant-050213-040000
10.1071/PP9860699
10.1016/J.FCR.2020.107945
10.1186/S12870-020-02401-8/FIGURES/5
10.1111/NPH.15344
10.1038/s41586-020-03127-1
10.2135/cropsci2013.04.0271
10.1038/s41586-020-3016-z
10.2135/CROPSCI2012.11.0641
10.1242/DEV.040931
10.1016/j.ajhg.2018.07.015
10.1038/cr.2009.108
10.1007/S11103-006-9089-8/TABLES/1
10.1007/S10681-013-1005-0/TABLES/6
10.1073/pnas.1222368110
10.1007/s11032-015-0240-6
10.1101/gr.089516.108
10.1007/S00438-019-01553-Z/FIGURES/6
10.1007/BF00012852
10.2135/cropsci2002.7390
10.1111/NPH.18704
10.2135/cropsci2017.03.0160
10.1007/s00122-018-3056-z
10.3389/FGENE.2016.00221
10.1016/j.ecolind.2018.03.003
10.3389/FPLS.2020.590740/BIBTEX
10.1186/S12864-016-2420-0/FIGURES/10
10.1016/J.EJA.2023.126745
10.1071/PP9860803
10.1111/PCE.13804
10.2135/CROPSCI1971.0011183X001100060051X
10.1007/S00122-019-03284-6/FIGURES/1
10.1016/S1360-1385(01)01889-1
10.1038/s41467-020-16968-1
10.1371/JOURNAL.PONE.0167962
10.1104/PP.66.1.61
ContentType Journal Article
Copyright Copyright © 2023 Arifuzzaman, Mamidi, Sanz-Saez, Zakeri, Scaboo and Fritschi 2023 Arifuzzaman, Mamidi, Sanz-Saez, Zakeri, Scaboo and Fritschi
Copyright_xml – notice: Copyright © 2023 Arifuzzaman, Mamidi, Sanz-Saez, Zakeri, Scaboo and Fritschi 2023 Arifuzzaman, Mamidi, Sanz-Saez, Zakeri, Scaboo and Fritschi
DBID AAYXX
CITATION
7X8
5PM
DOA
DOI 10.3389/fpls.2023.1271849
DatabaseName CrossRef
MEDLINE - Academic
PubMed Central (Full Participant titles)
DOAJ Directory of Open Access Journals
DatabaseTitle CrossRef
MEDLINE - Academic
DatabaseTitleList MEDLINE - Academic
CrossRef
Database_xml – sequence: 1
  dbid: DOA
  name: Directory of Open Access Journals
  url: http://www.doaj.org/
  sourceTypes: Open Website
DeliveryMethod fulltext_linktorsrc
Discipline Botany
EISSN 1664-462X
EndPage 1271849
ExternalDocumentID oai_doaj_org_article_a6bf7c6dd2604f6b86a1ce8fb6aada98
10_3389_fpls_2023_1271849
GroupedDBID 5VS
9T4
AAFWJ
AAKDD
AAYXX
ACGFO
ACGFS
ACXDI
ADBBV
ADRAZ
AENEX
AFPKN
ALMA_UNASSIGNED_HOLDINGS
AOIJS
BCNDV
CITATION
EBD
ECGQY
GROUPED_DOAJ
GX1
HYE
IAO
IEA
IGS
ISR
KQ8
M48
M~E
OK1
PGMZT
RNS
RPM
7X8
5PM
ID FETCH-LOGICAL-c395t-56fbcba3154803b722d84a61d55d8af8e6a980487542e3ded7faea3f17e565c83
IEDL.DBID RPM
ISSN 1664-462X
IngestDate Tue Oct 22 15:13:02 EDT 2024
Tue Sep 17 21:30:00 EDT 2024
Fri Oct 25 22:44:27 EDT 2024
Thu Sep 26 16:31:08 EDT 2024
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Language English
License This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c395t-56fbcba3154803b722d84a61d55d8af8e6a980487542e3ded7faea3f17e565c83
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
Reviewed by: Oswaldo Valdes-Lopez, National Autonomous University of Mexico, Mexico; Reetika Mahajan, University of Toledo, United States; Nonoy Bandillo, North Dakota State University, United States
Edited by: Babu Valliyodan, Lincoln University, United States
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10687445/
PQID 2896807060
PQPubID 23479
PageCount 1
ParticipantIDs doaj_primary_oai_doaj_org_article_a6bf7c6dd2604f6b86a1ce8fb6aada98
pubmedcentral_primary_oai_pubmedcentral_nih_gov_10687445
proquest_miscellaneous_2896807060
crossref_primary_10_3389_fpls_2023_1271849
PublicationCentury 2000
PublicationDate 2023-11-16
PublicationDateYYYYMMDD 2023-11-16
PublicationDate_xml – month: 11
  year: 2023
  text: 2023-11-16
  day: 16
PublicationDecade 2020
PublicationTitle Frontiers in plant science
PublicationYear 2023
Publisher Frontiers Media S.A
Publisher_xml – name: Frontiers Media S.A
References Wang (B128) 2016; 11
Kohl (B67) 1980; 66
Holland (B50) 2003; 22
Tabata (B122) 2014; 346
Caine (B17) 2023; 237
Bazzer (B6) 2020; 60
Bondari (B10) 2003
Lovell (B77) 2021; 590
Liyanage (B76) 2023; 12
Ni (B90) 2022; 12
Sharp (B111) 2017
Çağirgan (B14) 2005; 41
Bourion (B12) 2010; 121
Condon (B22) 2002; 42
Kunert (B70) 2016; 7
Ray (B101) 2015; 5
Wang (B127) 2018; 9
Yang (B135) 2019; 10
Dhanapal (B29) 2015; 8
Huo (B54); 6
Song (B119) 2020; 40
Adiredjo (B2) 2014; 9
Sanz‐Saez (B109) 2019; 59
Gan (B42) 2005; 222
Dong (B32) 2020; 589
Laffont (B71) 2020; 11
Robinson (B104) 1991; 6
Pasley (B93) 2020; 11
Fang (B39) 2020; 11
Purcell (B99) 2007; 81
Fehr (B41) 1971; 11
Kumarasinghe (B69) 1992; 139
Cafaro La Menza (B15) 2020; 43
Abrash (B1) 2010; 137
Lindemann (B73) 1979; 43
Sinclair (B115) 1987; 79
Ohlson (B91) 2018; 58
Farquhar (B40) 1989; 40
Bacanamwo (B5) 1996; 98
Cafaro La Menza (B16) 2017; 213
Coruzzi (B25) 2001; 4
Imin (B57) 2013; 64
Montañez (B88) 1995; 2
Luo (B79) 2019; 10
Torkamaneh (B123) 2018; 131
Xu (B132) 2015; 35
Djekoun (B30) 1991; 83
Hwang (B55) 2013; 53
Mariotti (B83) 1983; 303
Sinclair (B113) 1989; 29
Ma (B80) 2019; 20
Xu (B134) 2013; 110
Goodwin (B44) 2016; 17
Kaler (B59) 2017; 57
Sinha (B117) 2021; 311
Zhu (B139) 2019; 294
Coleto (B21) 2014; 113
Delay (B27) 2013; 64
Martynenko (B84) 2016; 5
Sall (B106) 1991; 133
O’Leary (B92) 1981; 20
Zhu (B138) 2016; 6
White (B129) 1996
Sinclair (B116) 2000; 40
Xu (B133) 2021; 167
King (B65) 2014; 54
Hubick (B53) 1986; 13
Lu (B78) 2007; 63
Bazzer (B7) 2020; 133
Kaler (B58) 2020; 10
Chen (B19) 2007; 1
Hu (B51) 2014; 65
Durand (B34) 1987; 38
Li (B72) 2008; 117
King (B62) 2001; 41
Zhang (B137) 2018; 871
Elsheikh (B37) 1995; 27
Song (B118) 2013; 8
Xiong (B131) 2021; 172
Peoples (B95) 2002
Steketee (B121) 2019; 20
Purcell (B98) 1997; 196
Gurung (B45) 2014; 9
Huang (B52) 2009; 19
Liu (B74) 2016; 12
Cingolani (B20) 2012; 6
Easlon (B35) 2014; 119
Kohl (B66) 1981; 60
Specht (B120) 2001; 41
Hall (B46) 1990; 30
Tripathi (B124) 2016; 17
Wu (B130) 2009; 19
Donahue (B31) 2020; 259
Sinclair (B114) 2010; 102
Piepho (B96) 2008; 161
Purcell (B97) 2015
Shearer (B112) 1986; 13
Sallam (B107) 2019; 20
Browning (B13) 2018; 103
Giehl (B43) 2017; 10
Vadez (B126) 2001; 52
Bazzer (B8) 2020; 216
Rotundo (B105) 2014; 54
Boudhrioua (B11) 2020; 20
Caine (B18) 2019; 221
Ayra (B4) 2021; 12
Rebetzke (B102) 2002; 42
Delaneau (B26) 2017; 8
Zhang (B136) 2015; 10
Mamidi (B82) 2014; 9
Richards (B103) 2002; 42
Hwang (B56) 2014; 195
Seck (B110) 2020; 11
Santos (B108) 2013; 150
Kumar (B68) 2015; 36
Arifuzzaman (B3) 2019; 294
King (B64) 2006; 46
Vadez (B125) 2016; 193
Purcell (B100) 2004; 44
Bhat (B9) 2016; 7
King (B63) 2005; 137
Liu (B75) 2016; 17
Ehleringer (B36) 1991; 31
Evans (B38) 2001; 6
Contreras-Soto (B23) 2017; 213
Harreman (B48) 2004; 14
Pazdernik (B94) 1997; 37
Moro Rosso (B89) 2023; 144
Harper (B47) 1987
Kim (B61) 2019; 35
Dhanapal (B28) 2015; 128
Mohammed (B87) 2019; 9
Kamfwa (B60) 2019; 132
Coruzzi (B24) 2001; 125
Dubey (B33) 2019; 105
Meyer (B85) 2013; 93
Heilig (B49) 2017; 57
MacAlister (B81) 2006; 445
Moghaddam (B86) 2016; 9
References_xml – volume: 9
  year: 2014
  ident: B2
  article-title: Genetic control of water use efficiency and leaf carbon isotope discrimination in sunflower (Helianthus annuus L.) subjected to two drought scenarios
  publication-title: PloS One
  doi: 10.1371/journal.pone.0101218
  contributor:
    fullname: Adiredjo
– year: 1996
  ident: B129
  article-title: The potential to use carbon isotope discrimination as a selection tool to improve water-use efficiency in Soybean
  contributor:
    fullname: White
– volume: 125
  start-page: 61
  year: 2001
  ident: B24
  article-title: Nitrogen and carbon nutrient and metabolite signaling in plants
  publication-title: Plant Physiol.
  doi: 10.1104/PP.125.1.61
  contributor:
    fullname: Coruzzi
– volume: 9
  year: 2016
  ident: B86
  article-title: Genome-wide association study identifies candidate loci underlying agronomic traits in a middle american diversity panel of common bean
  publication-title: Plant Genome
  doi: 10.3835/plantgenome2016.02.0012
  contributor:
    fullname: Moghaddam
– volume: 52
  start-page: 153
  year: 2001
  ident: B126
  article-title: Leaf ureide degradation and N(2) fixation tolerance to water deficit in soybean
  publication-title: J. Exp. Bot.
  doi: 10.1093/jxb/erh100
  contributor:
    fullname: Vadez
– volume: 41
  start-page: 229
  year: 2005
  ident: B14
  article-title: Genotypic variability for carbon isotope discrimination in the mutant and improved lines of barley
  publication-title: Isot. in Env. and Health Stud.
  doi: 10.1080/10256010500230106
  contributor:
    fullname: Çağirgan
– volume: 6
  start-page: 80
  year: 2012
  ident: B20
  article-title: A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3
  publication-title: Fly (Austin)
  doi: 10.4161/FLY.19695
  contributor:
    fullname: Cingolani
– volume: 58
  start-page: 264
  year: 2018
  ident: B91
  article-title: QTL mapping of ineffective nodulation and nitrogen utilization-related traits in the IC-1 mutant of cowpea
  publication-title: Crop Sci.
  doi: 10.2135/CROPSCI2017.07.0439
  contributor:
    fullname: Ohlson
– volume: 30
  start-page: 300
  year: 1990
  ident: B46
  article-title: Genotypic differences in carbon isotope discrimination by cowpea under wet and dry field conditions
  publication-title: Crop Sci.
  doi: 10.2135/CROPSCI1990.0011183X003000020011X
  contributor:
    fullname: Hall
– volume: 10
  year: 2019
  ident: B79
  article-title: Editorial: Crop breeding for drought resistance
  publication-title: Front. Plant Sci.
  doi: 10.3389/FPLS.2019.00314/BIBTEX
  contributor:
    fullname: Luo
– volume: 5
  start-page: 2391
  year: 2015
  ident: B101
  article-title: Genome-wide association study of ureide concentration in diverse maturity group IV soybean [Glycine max (L.) merr.] accessions
  publication-title: G3 (Bethesda)
  doi: 10.1534/G3.115.021774
  contributor:
    fullname: Ray
– volume: 196
  start-page: 101
  year: 1997
  ident: B98
  article-title: Biomass accumulation and allocation in soybean associated with genotypic differences in tolerance of nitrogen fixation to water deficits
  publication-title: Plant Soil
  doi: 10.1023/A:1004289609466
  contributor:
    fullname: Purcell
– volume: 54
  start-page: 1153
  year: 2014
  ident: B105
  article-title: Soybean nitrogen uptake and utilization in Argentina and United States cultivars
  publication-title: Crop Sci.
  doi: 10.2135/CROPSCI2013.09.0618
  contributor:
    fullname: Rotundo
– volume: 43
  start-page: 1134
  year: 1979
  ident: B73
  article-title: Soybean plant growth, nodulation, and nitrogen fixation as affected by root temperature
  publication-title: Soil Sci. Soc. America J.
  doi: 10.2136/SSSAJ1979.03615995004300060014X
  contributor:
    fullname: Lindemann
– volume: 121
  start-page: 71
  year: 2010
  ident: B12
  article-title: Genetic dissection of nitrogen nutrition in pea through a QTL approach of root, nodule, and shoot variability
  publication-title: Theor. Appl. Genet.
  doi: 10.1007/S00122-010-1292-Y/FIGURES/5
  contributor:
    fullname: Bourion
– volume: 119
  start-page: 119
  year: 2014
  ident: B35
  article-title: The physiological basis for genetic variation in water use efficiency and carbon isotope composition in Arabidopsis thaliana
  publication-title: Photosynth Res.
  doi: 10.1007/s11120-013-9891-5
  contributor:
    fullname: Easlon
– volume: 35
  start-page: 4419
  year: 2019
  ident: B61
  article-title: gpart: human genome partitioning and visualization of high-density SNP data by identifying haplotype blocks
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btz308
  contributor:
    fullname: Kim
– volume: 303
  start-page: 685
  year: 1983
  ident: B83
  article-title: Atmospheric nitrogen is a reliable standard for natural 15N abundance measurements
  publication-title: Nat. 1983
  doi: 10.1038/303685a0
  contributor:
    fullname: Mariotti
– volume: 59
  start-page: 2153
  year: 2019
  ident: B109
  article-title: Using carbon isotope discrimination to assess genotypic differences in drought resistance of parental lines of common bean
  publication-title: Crop Sci.
  doi: 10.2135/cropsci2019.02.0085
  contributor:
    fullname: Sanz‐Saez
– volume: 10
  year: 2019
  ident: B135
  article-title: Genetic analysis and mapping of QTLs for soybean biological nitrogen fixation traits under varied field conditions
  publication-title: Front. Plant Sci.
  doi: 10.3389/FPLS.2019.00075/BIBTEX
  contributor:
    fullname: Yang
– volume: 113
  start-page: 1071
  year: 2014
  ident: B21
  article-title: Comparison of inhibition of N2 fixation and ureide accumulation under water deficit in four common bean genotypes of contrasting drought tolerance
  publication-title: Ann. Bot.
  doi: 10.1093/AOB/MCU029
  contributor:
    fullname: Coleto
– volume: 93
  start-page: 1046
  year: 2013
  ident: B85
  article-title: Fine-scale mapping of the FGFR2 breast cancer risk locus: Putative functional variants differentially bind FOXA1 and E2F1
  publication-title: Am. J. Hum. Genet.
  doi: 10.1016/j.ajhg.2013.10.026
  contributor:
    fullname: Meyer
– volume: 10
  start-page: 5166
  year: 2020
  ident: B58
  article-title: Genome-wide association mapping of dark green color index using a diverse panel of soybean accessions
  publication-title: Sci. Rep.
  doi: 10.1038/s41598-020-62034-7
  contributor:
    fullname: Kaler
– volume: 17
  start-page: 333
  year: 2016
  ident: B44
  article-title: Coming of age: Ten years of next-generation sequencing technologies
  publication-title: Nat. Rev. Genet.
  doi: 10.1038/nrg.2016.49
  contributor:
    fullname: Goodwin
– volume: 172
  start-page: 405
  year: 2021
  ident: B131
  article-title: Root system architecture, physiological and transcriptional traits of soybean (Glycine max L.) in response to water deficit: A review
  publication-title: Physiol. Plant
  doi: 10.1111/PPL.13201
  contributor:
    fullname: Xiong
– volume: 57
  start-page: 118
  year: 2017
  ident: B49
  article-title: QTL analysis of symbiotic nitrogen fixation in a black bean population
  publication-title: Crop Sci.
  doi: 10.2135/CROPSCI2016.05.0348
  contributor:
    fullname: Heilig
– volume: 41
  start-page: 493
  year: 2001
  ident: B120
  article-title: Soybean response to water: A QTL analysis of drought tolerance
  publication-title: Crop Sci.
  doi: 10.2135/CROPSCI2001.412493X
  contributor:
    fullname: Specht
– volume: 167
  start-page: 980
  year: 2021
  ident: B133
  article-title: The soybean CBL-interacting protein kinase, GmCIPK2, positively regulates drought tolerance and ABA signaling
  publication-title: Plant Physiol. Biochem.
  doi: 10.1016/J.PLAPHY.2021.09.026
  contributor:
    fullname: Xu
– volume: 12
  year: 2022
  ident: B90
  article-title: Mapping of Quantitative Trait Loci Underlying Nodule Traits in Soybean (Glycine max (L.) Merr.) and Identification of Genes Whose Expression Is Affected by the Sinorhizobium fredii HH103 Effector Proteins NopL and NopT
  publication-title: Agronomy
  doi: 10.3390/AGRONOMY12040946/S1
  contributor:
    fullname: Ni
– volume: 20
  start-page: 3137 20, 3137
  year: 2019
  ident: B107
  article-title: Drought stress tolerance in wheat and barley: advances in physiology, breeding and genetics research
  publication-title: Int. J. Mol. Sci.
  doi: 10.3390/IJMS20133137
  contributor:
    fullname: Sallam
– volume: 871
  year: 2018
  ident: B137
  article-title: Identification of QTNs controlling seed protein content in soybean using multi-locus genome-wide association studies
  publication-title: Front. Plant Sci.
  doi: 10.3389/FPLS.2018.01690/BIBTEX
  contributor:
    fullname: Zhang
– volume: 11
  year: 2020
  ident: B39
  article-title: Linkage analysis and multi-locus genome-wide association studies identify QTNs controlling soybean plant height
  publication-title: Front. Plant Sci.
  doi: 10.3389/FPLS.2020.00009/BIBTEX
  contributor:
    fullname: Fang
– volume: 14
  start-page: 505
  year: 2004
  ident: B48
  article-title: Importin alpha: a multipurpose nuclear-transport receptor
  publication-title: Trends Cell Biol.
  doi: 10.1016/j.tcb.2004.07.016
  contributor:
    fullname: Harreman
– volume: 41
  start-page: 1099
  year: 2001
  ident: B62
  article-title: Soybean nodule size and relationship to nitrogen fixation response to water deficit
  publication-title: Crop Sci.
  doi: 10.2135/CROPSCI2001.4141099X
  contributor:
    fullname: King
– volume: 20
  start-page: 811
  year: 2019
  ident: B121
  article-title: Unraveling the genetic architecture for carbon and nitrogen related traits and leaf hydraulic conductance in soybean using genome-wide association analyses
  publication-title: BMC Genomics
  doi: 10.1186/s12864-019-6170-7
  contributor:
    fullname: Steketee
– volume: 150
  start-page: 17
  year: 2013
  ident: B108
  article-title: Mapping of QTLs associated with biological nitrogen fixation traits in soybean
  publication-title: Hereditas
  doi: 10.1111/J.1601-5223.2013.02275.X
  contributor:
    fullname: Santos
– volume: 22
  start-page: 9
  year: 2003
  ident: B50
  article-title: Estimating and interpreting heritability for plant breeding: an update
  publication-title: Plant Breed Rev.
  doi: 10.1002/9780470650202.ch2
  contributor:
    fullname: Holland
– volume: 8
  year: 2017
  ident: B26
  article-title: A complete tool set for molecular QTL discovery and analysis
  publication-title: Nat. Commun.
  doi: 10.1038/ncomms15452
  contributor:
    fullname: Delaneau
– volume: 4
  start-page: 247
  year: 2001
  ident: B25
  article-title: Carbon and nitrogen sensing and signaling in plants: Emerging “matrix effects”
  publication-title: Curr. Opin. Plant Biol
  doi: 10.1016/S1369-5266(00)00168-0
  contributor:
    fullname: Coruzzi
– volume: 9
  start-page: 1
  year: 2019
  ident: B87
  article-title: Rice plants overexpressing OsEPF1 show reduced stomatal density and increased root cortical aerenchyma formation
  publication-title: Sci. Rep.
  doi: 10.1038/s41598-019-41922-7
  contributor:
    fullname: Mohammed
– volume: 60
  start-page: 2479
  year: 2020
  ident: B6
  article-title: Mapping and confirmation of quantitative trait loci (QTLs) associated with carbon isotope ratio (δ13C) in soybean
  publication-title: Crop Sci.
  doi: 10.1002/csc2.20240
  contributor:
    fullname: Bazzer
– volume: 36
  start-page: 1011
  year: 2015
  ident: B68
  article-title: Molecular analysis of soybean varying in water use efficiency using SSRs markers
  publication-title: J. Environ. Biol.
  doi: 10.1007/s11033-021-07030-4
  contributor:
    fullname: Kumar
– volume: 102
  start-page: 475
  year: 2010
  ident: B114
  article-title: Assessment across the United States of the benefits of altered soybean drought traits
  publication-title: Agron. J.
  doi: 10.2134/AGRONJ2009.0195
  contributor:
    fullname: Sinclair
– volume: 40
  start-page: 1803
  year: 2000
  ident: B116
  article-title: Identification of soybean genotypes with N2 fixation tolerance to water deficits
  publication-title: Crop Sci.
  doi: 10.2135/CROPSCI2000.4061803X
  contributor:
    fullname: Sinclair
– volume: 222
  start-page: 730
  year: 2005
  ident: B42
  article-title: Nutritional regulation of ANR1 and other root-expressed MADS-box genes in Arabidopsis thaliana
  publication-title: Planta
  doi: 10.1007/S00425-005-0020-3
  contributor:
    fullname: Gan
– volume: 64
  start-page: 5395
  year: 2013
  ident: B57
  article-title: The peptide-encoding CEP1 gene modulates lateral root and nodule numbers in Medicago truncatula
  publication-title: J. Exp. Bot.
  doi: 10.1093/JXB/ERT369
  contributor:
    fullname: Imin
– start-page: 357
  volume-title: The Nitrogen Fixation at Millennium
  year: 2002
  ident: B95
  article-title: Quantification of nitrogen fixation
  doi: 10.1016/B978-044450965-9/50013-6
  contributor:
    fullname: Peoples
– volume: 12
  year: 2021
  ident: B4
  article-title: Control of the rhizobia nitrogen-fixing symbiosis by common bean MADS-Domain/AGL transcription factors
  publication-title: Front. Plant Sci.
  doi: 10.3389/fpls.2021.679463
  contributor:
    fullname: Ayra
– volume: 42
  start-page: 122
  year: 2002
  ident: B22
  article-title: Improving intrinsic water-use efficiency and crop yield
  publication-title: Crop Sci.
  doi: 10.2135/cropsci2002.1220
  contributor:
    fullname: Condon
– volume: 137
  start-page: 1389
  year: 2005
  ident: B63
  article-title: Inhibition of N2 fixation in soybean is associated with elevated ureides and amino acids
  publication-title: Plant Physiol.
  doi: 10.1104/PP.104.056317
  contributor:
    fullname: King
– volume: 40
  start-page: 1
  year: 2020
  ident: B119
  article-title: Identification of QTL and genes for pod number in soybean by linkage analysis and genome-wide association studies
  publication-title: Mol. Breed.
  doi: 10.1007/S11032-020-01140-W/FIGURES/2
  contributor:
    fullname: Song
– start-page: 22
  year: 2003
  ident: B10
  article-title: Statistical analysis of genotype × environment interaction in agricultural research
  contributor:
    fullname: Bondari
– volume: 12
  year: 2016
  ident: B74
  article-title: Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies
  publication-title: PloS Genet.
  doi: 10.1371/journal.pgen.1005767
  contributor:
    fullname: Liu
– volume: 81
  start-page: 559
  year: 2007
  ident: B99
  article-title: PLINK: A tool set for whole-genome association and population-based linkage analyses
  publication-title: Am. J. Hum. Genet.
  doi: 10.1086/519795
  contributor:
    fullname: Purcell
– volume: 193
  start-page: 16
  year: 2016
  ident: B125
  article-title: High transpiration efficiency increases pod yield under intermittent drought in dry and hot atmospheric conditions but less so under wetter and cooler conditions in groundnut (Arachis hypogaea (L.))
  publication-title: Field Crops Res.
  doi: 10.1016/j.fcr.2016.03.001
  contributor:
    fullname: Vadez
– volume: 98
  start-page: 529
  year: 1996
  ident: B5
  article-title: Regulation of nitrogenase activity in Bradyrhizobium japonicum/soybean symbiosis by plant N status as determined by shoot C:N ratio
  publication-title: Physiol. Plant
  doi: 10.1111/J.1399-3054.1996.TB05708.X
  contributor:
    fullname: Bacanamwo
– volume: 8
  year: 2015
  ident: B29
  article-title: Genome-wide association analysis of diverse soybean genotypes reveals novel markers for nitrogen traits
  publication-title: Plant Genome
  doi: 10.3835/plantgenome2014.11.0086
  contributor:
    fullname: Dhanapal
– volume: 11
  year: 2020
  ident: B93
  article-title: Modeling flood-induced stress in soybeans
  publication-title: Front. Plant Sci.
  doi: 10.3389/FPLS.2020.00062/BIBTEX
  contributor:
    fullname: Pasley
– volume: 20
  start-page: 553
  year: 1981
  ident: B92
  article-title: Carbon isotope fractionation in plants
  publication-title: Phytochemistry
  doi: 10.1016/0031-9422(81)85134-5
  contributor:
    fullname: O’Leary
– start-page: 211
  year: 2015
  ident: B97
  contributor:
    fullname: Purcell
– volume: 20
  start-page: 2422
  year: 2019
  ident: B80
  article-title: The kinase CIPK11 functions as a negative regulator in drought stress response in arabidopsis
  publication-title: Int. J. Mol. Sci.
  doi: 10.3390/ijms20102422
  contributor:
    fullname: Ma
– volume: 40
  start-page: 503
  year: 1989
  ident: B40
  article-title: Carbon isotope discrimination and photosynthesis
  publication-title: Annu. Rev. Plant Physiol. Plant Mol. Biol.
  doi: 10.1146/annurev.pp.40.060189.002443
  contributor:
    fullname: Farquhar
– volume: 117
  start-page: 857
  year: 2008
  ident: B72
  article-title: Genetic structure and diversity of cultivated soybean (Glycine max (L.) Merr.) landraces in China
  publication-title: Theor. Appl. Genet.
  doi: 10.1007/s00122-008-0825-0
  contributor:
    fullname: Li
– volume: 10
  year: 2015
  ident: B136
  article-title: Genome-wide survey of the soybean GATA transcription factor gene family and expression analysis under low nitrogen stress
  publication-title: PloS One
  doi: 10.1371/journal.pone.0125174
  contributor:
    fullname: Zhang
– volume: 31
  start-page: 1611
  year: 1991
  ident: B36
  article-title: Carbon isotope discrimination and transpiration efficiency in common bean
  publication-title: Crop Sci.
  doi: 10.2135/cropsci1991.0011183x003100060046x
  contributor:
    fullname: Ehleringer
– volume: 128
  start-page: 73
  year: 2015
  ident: B28
  article-title: Genome-wide association study (GWAS) of carbon isotope ratio (δ13C) in diverse soybean [Glycine max (L.) Merr.] genotypes
  publication-title: Theor. Appl. Genet.
  doi: 10.1007/s00122-014-2413-9
  contributor:
    fullname: Dhanapal
– volume: 216
  start-page: 191
  year: 2020
  ident: B8
  article-title: Mapping quantitative trait loci (QTL) for plant nitrogen isotope ratio (δ15N) in soybean
  publication-title: Euphytica
  doi: 10.1007/s10681-020-02726-3
  contributor:
    fullname: Bazzer
– volume: 44
  start-page: 484
  year: 2004
  ident: B100
  article-title: Soybean N2 fixation estimates, ureide concentration, and yield responses to drought
  publication-title: Crop Sci.
  doi: 10.2135/cropsci2004.4840
  contributor:
    fullname: Purcell
– volume: 133
  start-page: 31
  year: 1991
  ident: B106
  article-title: Soybean genotypic differences in sensitivity of symbiotic nitrogen fixation to soil dehydration
  publication-title: Plant Soil
  doi: 10.1007/BF00011896
  contributor:
    fullname: Sall
– volume: 9
  year: 2014
  ident: B82
  article-title: Genome-wide association studies identifies seven major regions responsible for iron deficiency chlorosis in soybean (Glycine max)
  publication-title: PloS One
  doi: 10.1371/journal.pone.0107469
  contributor:
    fullname: Mamidi
– volume: 161
  start-page: 209
  year: 2008
  ident: B96
  article-title: BLUP for phenotypic selection in plant breeding and variety testing
  publication-title: Euphytica
  doi: 10.1007/S10681-007-9449-8/FIGURES/4
  contributor:
    fullname: Piepho
– volume: 7
  year: 2016
  ident: B70
  article-title: Drought stress responses in soybean roots and nodules
  publication-title: Front. Plant Sci.
  doi: 10.3389/fpls.2016.01015
  contributor:
    fullname: Kunert
– volume: 27
  start-page: 657
  year: 1995
  ident: B37
  article-title: Nodulation and N2 fixation by soybean inoculated with salt-tolerant rhizobia or salt-sensitive bradyrhizobia in saline soil
  publication-title: Soil Biol. Biochem.
  doi: 10.1016/0038-0717(95)98645-5
  contributor:
    fullname: Elsheikh
– volume: 9
  year: 2018
  ident: B127
  article-title: Genotyping of soybean cultivars with medium-density array reveals the population structure and QTNs underlying maturity and seed traits
  publication-title: Front. Plant Sci.
  doi: 10.3389/fpls.2018.00610
  contributor:
    fullname: Wang
– volume: 79
  start-page: 986
  year: 1987
  ident: B115
  article-title: Relative sensitivity of nitrogen and biomass accumulation to drought in field‐Grown soybean 1
  publication-title: Agron. J.
  doi: 10.2134/agronj1987.00021962007900060007x
  contributor:
    fullname: Sinclair
– volume: 213
  start-page: 173
  year: 2017
  ident: B23
  article-title: Population structure, genetic relatedness and linkage disequilibrium blocks in cultivars of tropical soybean (Glycine max)
  publication-title: Euphytica
  doi: 10.1007/s10681-017-1966-5
  contributor:
    fullname: Contreras-Soto
– volume: 64
  start-page: 5383
  year: 2013
  ident: B27
  article-title: CEP genes regulate root and shoot development in response to environmental cues and are specific to seed plants
  publication-title: J. Exp. Bot.
  doi: 10.1093/JXB/ERT332
  contributor:
    fullname: Delay
– volume: 445
  start-page: 537
  year: 2006
  ident: B81
  article-title: Transcription factor control of asymmetric cell divisions that establish the stomatal lineage
  publication-title: Nat. 2006
  doi: 10.1038/nature05491
  contributor:
    fullname: MacAlister
– volume: 5
  start-page: 1393
  year: 2016
  ident: B84
  article-title: Thermal imaging of soybean response to drought stress: the effect of Ascophyllum nodosum seaweed extract
  publication-title: Springerplus
  doi: 10.1186/s40064-016-3019-2
  contributor:
    fullname: Martynenko
– volume: 8
  year: 2013
  ident: B118
  article-title: Development and evaluation of SoySNP50K, a high-density genotyping array for soybean
  publication-title: PloS One
  doi: 10.1371/JOURNAL.PONE.0054985
  contributor:
    fullname: Song
– volume: 6
  ident: B54
  article-title: Overexpression of the Maize psbA Gene enhances drought tolerance through regulating antioxidant system, photosynthetic capability, and stress defense Gene expression in tobacco
  publication-title: Front. Plant Sci.
  doi: 10.3389/FPLS.2015.01223/BIBTEX
  contributor:
    fullname: Huo
– volume: 29
  start-page: 90
  year: 1989
  ident: B113
  article-title: Leaf nitrogen, photosynthesis, and crop radiation use efficiency: A review
  publication-title: Crop Sci.
  doi: 10.2135/CROPSCI1989.0011183X002900010023X
  contributor:
    fullname: Sinclair
– volume: 294
  start-page: 985
  year: 2019
  ident: B3
  article-title: Shovelomics for phenotyping root architectural traits of rapeseed/canola (Brassica napus L.) and genome-wide association mapping
  publication-title: Mol. Genet. Genomics
  doi: 10.1007/s00438-019-01563-x
  contributor:
    fullname: Arifuzzaman
– volume: 346
  start-page: 343
  year: 2014
  ident: B122
  article-title: Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling
  publication-title: Science
  doi: 10.1126/science.1257800
  contributor:
    fullname: Tabata
– volume: 38
  start-page: 311
  year: 1987
  ident: B34
  article-title: Nitrogenase activity, photosynthesis and nodule water potential in soyabean plants experiencing water deprivation
  publication-title: J. Exp. Bot
  doi: 10.1093/jxb/38.2.311
  contributor:
    fullname: Durand
– volume: 311
  year: 2021
  ident: B117
  article-title: The impact of stress combination on reproductive processes in crops
  publication-title: Plant Sci.
  doi: 10.1016/J.PLANTSCI.2021.111007
  contributor:
    fullname: Sinha
– volume: 1
  start-page: 166
  year: 2007
  ident: B19
  article-title: Registration of soybean germplasm lines R01-416F and R01-581F for improved yield and nitrogen fixation under drought stress
  publication-title: J. Plant Regist.
  doi: 10.3198/jpr2007.01.0046crg
  contributor:
    fullname: Chen
– volume: 17
  start-page: 177
  year: 2016
  ident: B75
  article-title: PGen: Large-scale genomic variations analysis workflow and browser in SoyKB
  publication-title: BMC Bioinf.
  doi: 10.1186/s12859-016-1227-y
  contributor:
    fullname: Liu
– volume: 83
  start-page: 316
  year: 1991
  ident: B30
  article-title: Water status effect on dinitrogen fixation and photosynthesis in soybean
  publication-title: Agron. J.
  doi: 10.2134/AGRONJ1991.00021962008300020011X
  contributor:
    fullname: Djekoun
– volume: 2
  start-page: 165
  year: 1995
  ident: B88
  article-title: The effect of temperature on nodulation and nitrogen fixation by five Bradyrhizobium japonicum strains
  publication-title: Appl. Soil Ecol.
  doi: 10.1016/0929-1393(95)00052-M
  contributor:
    fullname: Montañez
– volume: 9
  year: 2014
  ident: B45
  article-title: Genome-wide association study reveals novel quantitative trait loci associated with resistance to multiple leaf spot diseases of spring wheat
  publication-title: PloS One
  doi: 10.1371/journal.pone.0108179
  contributor:
    fullname: Gurung
– volume: 12
  year: 2023
  ident: B76
  article-title: The Genotypic Variability among Short-Season Soybean Cultivars for Nitrogen Fixation under Drought Stress
  publication-title: Plants
  doi: 10.3390/PLANTS12051004/S1
  contributor:
    fullname: Liyanage
– volume: 133
  start-page: 2141
  year: 2020
  ident: B7
  article-title: Identification of quantitative trait loci for carbon isotope ratio (δ13C) in a recombinant inbred population of soybean
  publication-title: Theor. Appl. Genet.
  doi: 10.1007/s00122-020-03586-0
  contributor:
    fullname: Bazzer
– volume-title: Principles of Stable Isotope Geochemistry
  year: 2017
  ident: B111
  contributor:
    fullname: Sharp
– volume: 42
  start-page: 111
  year: 2002
  ident: B103
  article-title: Breeding opportunities for increasing the efficiency of water use and crop yield in temperate cereals
  publication-title: Crop Sci.
  doi: 10.2135/CROPSCI2002.1110
  contributor:
    fullname: Richards
– volume: 213
  start-page: 204
  year: 2017
  ident: B16
  article-title: Is soybean yield limited by nitrogen supply
  publication-title: Field Crops Res.
  doi: 10.1016/J.FCR.2017.08.009
  contributor:
    fullname: Cafaro La Menza
– volume: 6
  start-page: 15
  year: 1991
  ident: B104
  article-title: That BLUP is a good thing: the estimation of random effects
  publication-title: Statist. Sci.
  doi: 10.1214/SS/1177011926
  contributor:
    fullname: Robinson
– start-page: 497
  volume-title: Soybeans: Improvement, Production and Uses
  year: 1987
  ident: B47
  article-title: Nitrogen metabolism
  contributor:
    fullname: Harper
– volume: 60
  start-page: 487
  year: 1981
  ident: B66
  article-title: The use of soils lightly enriched in15N to screen for N2-fixing activity
  publication-title: Plant Soil
  doi: 10.1007/BF02149646/METRICS
  contributor:
    fullname: Kohl
– volume: 6
  year: 2016
  ident: B138
  article-title: Evolution of an intron-poor cluster of the CIPK gene family and expression in response to drought stress in soybean
  publication-title: Sci. Rep.
  doi: 10.1038/srep28225
  contributor:
    fullname: Zhu
– volume: 46
  start-page: 2396
  year: 2006
  ident: B64
  article-title: Genotypic variation for shoot N concentration and response to water deficits in soybean
  publication-title: Crop Sci.
  doi: 10.2135/cropsci2006.03.0165
  contributor:
    fullname: King
– volume: 10
  start-page: 1449
  year: 2017
  ident: B43
  article-title: A critical role of AMT2;1 in root-to-shoot translocation of ammonium in arabidopsis
  publication-title: Mol. Plant
  doi: 10.1016/J.MOLP.2017.10.001
  contributor:
    fullname: Giehl
– volume: 37
  start-page: 1482
  year: 1997
  ident: B94
  article-title: Variation in the pattern of nitrogen accumulation and distribution in soybean
  publication-title: Crop Sci.
  doi: 10.2135/CROPSCI1997.0011183X003700050011X
  contributor:
    fullname: Pazdernik
– volume: 65
  start-page: 715
  year: 2014
  ident: B51
  article-title: Genetic engineering and breeding of drought-resistant crops
  publication-title: Annu. Rev. Plant Biol.
  doi: 10.1146/annurev-arplant-050213-040000
  contributor:
    fullname: Hu
– volume: 13
  start-page: 699
  year: 1986
  ident: B112
  article-title: Nz-fixation in field settings: estimations based on natural "N abundance
  publication-title: Rev. Aust. J. Plant Physiol.
  doi: 10.1071/PP9860699
  contributor:
    fullname: Shearer
– volume: 259
  year: 2020
  ident: B31
  article-title: The quantity of nitrogen derived from symbiotic N fixation but not the relative contribution of N fixation to total N uptake increased with breeding for greater soybean yields
  publication-title: Field Crops Res.
  doi: 10.1016/J.FCR.2020.107945
  contributor:
    fullname: Donahue
– volume: 20
  start-page: 1
  year: 2020
  ident: B11
  article-title: Genome-wide association mapping of Sclerotinia sclerotiorum resistance in soybean using whole-genome resequencing data
  publication-title: BMC Plant Biol.
  doi: 10.1186/S12870-020-02401-8/FIGURES/5
  contributor:
    fullname: Boudhrioua
– volume: 221
  start-page: 371
  year: 2019
  ident: B18
  article-title: Rice with reduced stomatal density conserves water and has improved drought tolerance under future climate conditions
  publication-title: New Phytol.
  doi: 10.1111/NPH.15344
  contributor:
    fullname: Caine
– volume: 590
  start-page: 438
  year: 2021
  ident: B77
  article-title: Genomic mechanisms of climate adaptation in polyploid bioenergy switchgrass
  publication-title: Nature
  doi: 10.1038/s41586-020-03127-1
  contributor:
    fullname: Lovell
– volume: 54
  start-page: 746
  year: 2014
  ident: B65
  article-title: A possible relationship between shoot N concentration and the sensitivity of N2 fixation to drought in soybean
  publication-title: Crop Sci.
  doi: 10.2135/cropsci2013.04.0271
  contributor:
    fullname: King
– volume: 589
  start-page: 586
  year: 2020
  ident: B32
  article-title: An SHR–SCR module specifies legume cortical cell fate to enable nodulation
  publication-title: Nat. 2020 589:7843
  doi: 10.1038/s41586-020-3016-z
  contributor:
    fullname: Dong
– volume: 53
  start-page: 2421
  year: 2013
  ident: B55
  article-title: QTL analysis of shoot ureide and nitrogen concentrations in soybean [Glycine max (L.) merr.]
  publication-title: Crop Sci.
  doi: 10.2135/CROPSCI2012.11.0641
  contributor:
    fullname: Hwang
– volume: 137
  start-page: 447
  year: 2010
  ident: B1
  article-title: Regional specification of stomatal production by the putative ligand CHALLAH
  publication-title: Development
  doi: 10.1242/DEV.040931
  contributor:
    fullname: Abrash
– volume: 103
  start-page: 338
  year: 2018
  ident: B13
  article-title: A one-penny imputed genome from next-generation reference panels
  publication-title: Am. J. Hum. Genet.
  doi: 10.1016/j.ajhg.2018.07.015
  contributor:
    fullname: Browning
– volume: 19
  start-page: 1279
  year: 2009
  ident: B130
  article-title: Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses
  publication-title: Cell Res.
  doi: 10.1038/cr.2009.108
  contributor:
    fullname: Wu
– volume: 63
  start-page: 289
  year: 2007
  ident: B78
  article-title: A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress-responsive genes in Arabidopsis
  publication-title: Plant Mol. Biol.
  doi: 10.1007/S11103-006-9089-8/TABLES/1
  contributor:
    fullname: Lu
– volume: 195
  start-page: 419
  year: 2014
  ident: B56
  article-title: Genetics and mapping of quantitative traits for nodule number, weight, and size in soybean (Glycine max L.[Merr.])
  publication-title: Euphytica
  doi: 10.1007/S10681-013-1005-0/TABLES/6
  contributor:
    fullname: Hwang
– volume: 110
  start-page: 13469
  year: 2013
  ident: B134
  article-title: Pinpointing genes underlying the quantitative trait loci for root-knot nematode resistance in palaeopolyploid soybean by whole genome resequencing
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.1222368110
  contributor:
    fullname: Xu
– volume: 35
  start-page: 33
  year: 2015
  ident: B132
  article-title: Whole-genome resequencing: changing the paradigms of SNP detection, molecular mapping and gene discovery
  publication-title: Mol. Breed.
  doi: 10.1007/s11032-015-0240-6
  contributor:
    fullname: Xu
– volume: 19
  start-page: 1068
  year: 2009
  ident: B52
  article-title: High-throughput genotyping by whole-genome resequencing
  publication-title: Genome Res.
  doi: 10.1101/gr.089516.108
  contributor:
    fullname: Huang
– volume: 294
  start-page: 1049
  year: 2019
  ident: B139
  article-title: QTL analysis of nodule traits and the identification of loci interacting with the type III secretion system in soybean
  publication-title: Mol. Genet. Genomics
  doi: 10.1007/S00438-019-01553-Z/FIGURES/6
  contributor:
    fullname: Zhu
– volume: 139
  start-page: 145
  year: 1992
  ident: B69
  article-title: 13C isotope discrimination correlates with biological nitrogen fixation in soybean (Glycine max (L.) Merrill)
  publication-title: Plant Soil
  doi: 10.1007/BF00012852
  contributor:
    fullname: Kumarasinghe
– volume: 42
  start-page: 739
  year: 2002
  ident: B102
  article-title: Selection for reduced carbon isotope discrimination increases aerial biomass and grain yield of rainfed bread wheat
  publication-title: Crop Sci.
  doi: 10.2135/cropsci2002.7390
  contributor:
    fullname: Rebetzke
– volume: 237
  start-page: 2180
  year: 2023
  ident: B17
  article-title: The influences of stomatal size and density on rice abiotic stress resilience
  publication-title: New Phytol.
  doi: 10.1111/NPH.18704
  contributor:
    fullname: Caine
– volume: 57
  start-page: 3085
  year: 2017
  ident: B59
  article-title: Genome-wide association mapping of carbon isotope and oxygen isotope ratios in diverse soybean genotypes
  publication-title: Crop Sci.
  doi: 10.2135/cropsci2017.03.0160
  contributor:
    fullname: Kaler
– volume: 131
  start-page: 499
  year: 2018
  ident: B123
  article-title: Efficient genome-wide genotyping strategies and data integration in crop plants
  publication-title: Theor. Appl. Genet.
  doi: 10.1007/s00122-018-3056-z
  contributor:
    fullname: Torkamaneh
– volume: 7
  year: 2016
  ident: B9
  article-title: Genomic selection in the era of next generation sequencing for complex traits in plant breeding
  publication-title: Front. Genet.
  doi: 10.3389/FGENE.2016.00221
  contributor:
    fullname: Bhat
– volume: 105
  start-page: 425
  year: 2019
  ident: B33
  article-title: Growing more with less: Breeding and developing drought resilient soybean to improve food security
  publication-title: Ecol. Indic
  doi: 10.1016/j.ecolind.2018.03.003
  contributor:
    fullname: Dubey
– volume: 11
  year: 2020
  ident: B110
  article-title: Comprehensive genome-wide association analysis reveals the genetic basis of root system architecture in soybean
  publication-title: Front. Plant Sci.
  doi: 10.3389/FPLS.2020.590740/BIBTEX
  contributor:
    fullname: Seck
– volume: 17
  start-page: 1
  year: 2016
  ident: B124
  article-title: A toolbox of genes, proteins, metabolites and promoters for improving drought tolerance in soybean includes the metabolite coumestrol and stomatal development genes
  publication-title: BMC Genomics
  doi: 10.1186/S12864-016-2420-0/FIGURES/10
  contributor:
    fullname: Tripathi
– volume: 144
  year: 2023
  ident: B89
  article-title: Temporal variation of soil N supply defines N fixation in soybeans
  publication-title: Eur. J. Agron.
  doi: 10.1016/J.EJA.2023.126745
  contributor:
    fullname: Moro Rosso
– volume: 13
  start-page: 803
  year: 1986
  ident: B53
  article-title: Correlation between water-use efficiency and carbon isotope discrimination in diverse peanut (Arachis) germplasm
  publication-title: Funct. Plant Biol.
  doi: 10.1071/PP9860803
  contributor:
    fullname: Hubick
– volume: 43
  start-page: 1958
  year: 2020
  ident: B15
  article-title: Insufficient nitrogen supply from symbiotic fixation reduces seasonal crop growth and nitrogen mobilization to seed in highly productive soybean crops
  publication-title: Plant Cell Environ.
  doi: 10.1111/PCE.13804
  contributor:
    fullname: Cafaro La Menza
– volume: 11
  start-page: 929
  year: 1971
  ident: B41
  article-title: Stage of development descriptions for soybeans, glycine max (L.) merrill1
  publication-title: Crop Sci.
  doi: 10.2135/CROPSCI1971.0011183X001100060051X
  contributor:
    fullname: Fehr
– volume: 132
  start-page: 1375
  year: 2019
  ident: B60
  article-title: Identification of quantitative trait loci for symbiotic nitrogen fixation in common bean
  publication-title: Theor. Appl. Genet.
  doi: 10.1007/S00122-019-03284-6/FIGURES/1
  contributor:
    fullname: Kamfwa
– volume: 6
  start-page: 121
  year: 2001
  ident: B38
  article-title: Physiological mechanisms influencing plant nitrogen isotope composition
  publication-title: Trends Plant Sci.
  doi: 10.1016/S1360-1385(01)01889-1
  contributor:
    fullname: Evans
– volume: 11
  start-page: 1
  year: 2020
  ident: B71
  article-title: The NIN transcription factor coordinates CEP and CLE signaling peptides that regulate nodulation antagonistically
  publication-title: Nat. Commun.
  doi: 10.1038/s41467-020-16968-1
  contributor:
    fullname: Laffont
– volume: 11
  year: 2016
  ident: B128
  article-title: A CBL-interacting protein kinase taCIPK2 confers drought tolerance in transgenic tobacco plants through regulating the stomatal movement
  publication-title: PloS One
  doi: 10.1371/JOURNAL.PONE.0167962
  contributor:
    fullname: Wang
– volume: 66
  year: 1980
  ident: B67
  article-title: Estimates of N2 fixation based on differences in the natural abundance of 15N in nodulating and nonnodulating isolines of soybeans
  publication-title: Plant Physiol.
  doi: 10.1104/PP.66.1.61
  contributor:
    fullname: Kohl
SSID ssj0000500997
Score 2.4083714
Snippet Soybean ( Glycine max ) production is greatly affected by persistent and/or intermittent droughts in rainfed soybean-growing regions worldwide. Symbiotic N 2...
Soybean (Glycine max) production is greatly affected by persistent and/or intermittent droughts in rainfed soybean-growing regions worldwide. Symbiotic N2...
SourceID doaj
pubmedcentral
proquest
crossref
SourceType Open Website
Open Access Repository
Aggregation Database
StartPage 1271849
SubjectTerms carbon isotope ratio
genome-wide association mapping
nitrogen isotope ratio
Plant Science
water use efficiency
whole genome resequencing
SummonAdditionalLinks – databaseName: DOAJ Directory of Open Access Journals
  dbid: DOA
  link: http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1Lb9QwELag4sAFtTzEtlAZiRNSaGIntnOkL_XEBZC4RePHiEiQVLtdwf57ZuK02py4cIuSyHa-sTPz2Z7PQry3DVkVsCmQOkxRtyoVDlIsjLIBWAKtDDyne_PFfv7uLq9YJufhqC_eE5blgTNwZ2A82mBipMC7RuOdgSokh94ARGhzmm_p9shUVvXm0MfmZUxiYe0Z3v5kdW6lP1aK_sesnbnniCa9_kWQudwiuedzrg_FszlYlJ9yI4_EozQ8F0_ORwrodi8E5iRbnGfd5IiSPFMvYUY8RcmzrPI3Xa7ldpNkmvQiONlSwhDlZvfL9yOVLWlcr0fqShL7P7mwfpCbcecTDC_Ft-urrxc3xXxsQhF029wVjUEfPGgmI6X2VqnoajBVbJroAF0yBFvJRKVWSccULUICjZVNFN0Fp1-Jg2Ec0msh64hlrL225OQpslM-KiLfqH0Z6qbCsBIf7jHsbrM6RkesggHvGPCOAe9mwFfinFF-eJGFracbZO5uNnf3L3OvxLt7G3U0EHh1A4Y0bqkq1xpXshjQSriF8RY1Lp8M_Y9JUpuIMZ8D0Bz_jzaeiKf83ZyxWJk34uBuvU1vxeNN3J5OvfQvEWvyWA
  priority: 102
  providerName: Directory of Open Access Journals
Title Identification of loci associated with water use efficiency and symbiotic nitrogen fixation in soybean
URI https://search.proquest.com/docview/2896807060
https://pubmed.ncbi.nlm.nih.gov/PMC10687445
https://doaj.org/article/a6bf7c6dd2604f6b86a1ce8fb6aada98
Volume 14
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lj9MwEB7RFQcuiKcoj5WROCGlTezEdo7ssqu9gJAAiVvkJ0TaOlW7FfTfM5MHaq7cojxsZ2acmc-e-QLwTlWoVROrLKLBZGXNQ6ZN8JnkyhmiQMsdrenefFWff-iPV0STI6damD5p39l2lW43q9T-6nMrtxu3nvLE1l8-XSKMIdb2ar2ABQaHJxh9YPSmsEcNW5iIwOp13N4SMzcXq4Ljt5h4M0-cUM_VPwsw5-mRJ_7m-hE8HANF9mEY0GO4F9ITuH_RYTB3fApxKLCN44ob6yJDr9QyM0o7eEYrrOw3Hu7YYR9Y6LkiqNCSmeTZ_rixbYdtM5zTuw7NiMX2z9BYm9i-O9pg0jP4fn317fImG3-ZkDlRV3dZJaN11ggCIrmwinOvSyMLX1Vem6iDNLXOCaSUPAgfvIomGBELFTCyc1o8h7PUpfACWOlj7ksrFDp4jOq49RyBdxQ2d2VVRLeE95MMm-3AjNEgoiCBNyTwhgTejAJfwgVJ-d-NRGrdn-h2P5tRtY2RNionvUeMVUZptTSFCzpaaYzHcS_h7aSjBicB7WyYFLoDdqVrqXMiAlqCnilv1uP8ClpXT6c9WdPL_3_0FTygt6UaxUK-hrO73SG8gcXeH857kH_eW-hf-ivwew
link.rule.ids 230,315,729,782,786,866,887,2108,27935,27936,53803,53805
linkProvider National Library of Medicine
linkToHtml http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Jb9QwFLZoQYILZRUDFIzECSkziZ3YzpFuGkRbIVEkbpbXEqmTjGY6gvn3vJelmlx7i-LEdvx5eZ_93hdCPssCUDWxSCJ0mCQvWUiUCT4RTDqDEmipwz3d-U95-VudnKJMjhhiYVqnfWeraX2zmNbVn9a3crlws8FPbPbj4hhoDKq2F7M98hAGbMp3WHqn6Y2Gj-wOMYGDlbO4vEFtbsanGYPZGJUzd5ahVq1_ZGKOHSR3Vpyzg_vW9Rl52tuY9GuX_pw8CPUL8uioATtw-5LELjY39pt1tIkUFrSKmh6o4CluztK_cLmim3WgoZWZwBhNampP19uFrRrIm8J0sGqgB9JY_esyq2q6brY2mPoV-XV2enU8T_q_LSSOl8VtUohonTUcOUzKrWTMq9yIzBeFVyaqIEypUuQ3OQvcBy-jCYbHTAYwCp3ir8l-3dThDaG5j6nPLZdgG4BByKxnwNkjt6nLiyy6CfkyNL5edqIaGsgIIqURKY1I6R6pCTlCeO4eRD3s9kazutZ9S2sjbJROeA_0LI_CKmEyF1S0whgP9Z6QTwO4GsYPHoqYOjQbKEqVQqWoITQhaoT6qMRxCoDdKnEP4L69_6sfyeP51cW5Pv92-f0deYJfjqGOmXhP9m9Xm3BI9tZ-86Ht4P8BitYFVA
linkToPdf http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV3JjtQwELWYASEu7IhmNRInpHR2x-HGLK1BwGgkQOJmeash0rTT6p4W9N9TlQV1rnCLEsdLnpd6dtULY2-rElHVUEaAHSYq6sxHUnsXiayymiTQEkt7umdfq_Mf8uSUZHLej7EwndO-Nc08XC3nofnZ-VauljYe_cTiiy_HSGNItb2MVw7iA3YTB21S7jH1XtebjJ-qP8hEHlbHsLoife4sn6cZzsiknrm3FHWK_RMzc-okubfqLO79T33vs7uDrck_9GkesBs-PGS3jlq0B3ePGPQxujBs2vEWOC5sDdcDYN5x2qTlv_Byzbcbz30nN0GxmlwHxze7pWlazJvjtLBusSdyaH73mTWBb9qd8To8Zt8Xp9-Oz6LhrwuRzevyOioFGGt0TlwmyU2VZU4WWqSuLJ3UIL3QtUyI5xSZz513FWivc0grj8ahlfkTdhja4J8yXjhIXGHyCm0ENAwz4zLk7pCbxBZlCnbG3o0AqFUvrqGQlBBaitBShJYa0JqxI4Lob0LSxe5utOtLNXxtpYWBygrnkKYVIIwUOrVeghFaO6z3jL0ZAVY4juhwRAffbrEoWQuZkJbQjMkJ8pMSp08Q8E6RewT42b-_-prdvjhZqM8fzz89Z3eo4RTxmIoX7PB6vfUv2cHGbV91ffwPoj4H1A
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Identification+of+loci+associated+with+water+use+efficiency+and+symbiotic+nitrogen+fixation+in+soybean&rft.jtitle=Frontiers+in+plant+science&rft.au=Arifuzzaman%2C+Muhammad&rft.au=Mamidi%2C+Sujan&rft.au=Sanz-Saez%2C+Alvaro&rft.au=Zakeri%2C+Hossein&rft.date=2023-11-16&rft.issn=1664-462X&rft.eissn=1664-462X&rft.volume=14&rft.spage=1271849&rft.epage=1271849&rft_id=info:doi/10.3389%2Ffpls.2023.1271849&rft.externalDBID=NO_FULL_TEXT
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1664-462X&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1664-462X&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1664-462X&client=summon