Identification of genetic and environmental factors influencing aerial root traits that support biological nitrogen fixation in sorghum

Wolf, Emily S. A.; Vela, Saddie; Wilker, Jennifer; Davis, Alyssa; Robert, Madalen; Infante, Valentina; Venado, Rafael E.; Voiniciuc, Cătălin; Ané, Jean-Michel; Vermerris, Wilfred; Jamann, ed., T.

doi:10.1093/g3journal/jkad285

Title: Identification of genetic and environmental factors influencing aerial root traits that support biological nitrogen fixation in sorghum

Journal Article · 13 December 2023 · G3

DOI: https://doi.org/10.1093/g3journal/jkad285 · OSTI ID:2319259

;

; Davis, Alyssa;

;

; Jamann, ed., T.

Abstract Plant breeding and genetics play a major role in the adaptation of plants to meet human needs. The current requirement to make agriculture more sustainable can be partly met by a greater reliance on biological nitrogen fixation by symbiotic diazotrophic microorganisms that provide crop plants with ammonium. Select accessions of the cereal crop sorghum (Sorghum bicolor (L.) Moench) form mucilage-producing aerial roots that harbor nitrogen-fixing bacteria. Breeding programs aimed at developing sorghum varieties that support diazotrophs will benefit from a detailed understanding of the genetic and environmental factors contributing to aerial root formation. A genome-wide association study of the sorghum minicore, a collection of 242 landraces, and 30 accessions from the sorghum association panel was conducted in Florida and Wisconsin and under 2 fertilizer treatments to identify loci associated with the number of nodes with aerial roots and aerial root diameter. Sequence variation in genes encoding transcription factors that control phytohormone signaling and root system architecture showed significant associations with these traits. In addition, the location had a significant effect on the phenotypes. Concurrently, we developed F2 populations from crosses between bioenergy sorghums and a landrace that produced extensive aerial roots to evaluate the mode of inheritance of the loci identified by the genome-wide association study. Furthermore, the mucilage collected from aerial roots contained polysaccharides rich in galactose, arabinose, and fucose, whose composition displayed minimal variation among 10 genotypes and 2 fertilizer treatments. These combined results support the development of sorghums with the ability to acquire nitrogen via biological nitrogen fixation.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0021052

OSTI ID:: 2319259

Alternate ID(s):: OSTI ID: 2472373; OSTI ID: 2281296

Journal Information:: G3, Journal Name: G3 Journal Issue: 3 Vol. 14; ISSN 2160-1836

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (91)

Biological nitrogen fixation in field-grown sorghum under different edaphoclimatic conditions is confirmed by N isotopic signatures Barros, Benaia Gonçalves de França; Freitas, Ana Dolores Santiago de; Tabosa, José Nildo Nutrient Cycling in Agroecosystems, Vol. 117, Issue 1 https://doi.org/10.1007/s10705-020-10051-3	journal	February 2020
Analysis of Monosaccharides in Total Mucilage Extractable from Arabidopsis Seeds Voiniciuc, Cătălin; Günl, Markus BIO-PROTOCOL, Vol. 6, Issue 9 https://doi.org/10.21769/bioprotoc.1801	journal	January 2016
Functional characterization of the Arabidopsis transcription factor bZIP29 reveals its role in leaf and root development Van Leene, Jelle; Blomme, Jonas; Kulkarni, Shubhada R. Journal of Experimental Botany, Vol. 67, Issue 19 https://doi.org/10.1093/JXB/ERW347	journal	September 2016
The Mechanism of GT Element-mediated Cell Type-specific Transcriptional Control Villain, Patricia; Mache, Régis; Zhou, Dao-Xiu Journal of Biological Chemistry, Vol. 271, Issue 51 https://doi.org/10.1074/jbc.271.51.32593	journal	December 1996
Comprehensive Analysis of NAC Family Genes in Oryza sativa and Arabidopsis thaliana Ooka, H. DNA Research, Vol. 10, Issue 6 https://doi.org/10.1093/dnares/10.6.239	journal	January 2003
Biological nitrogen fixation: An efficient source of nitrogen for sustainable agricultural production? Peoples, M. B.; Herridge, D. F.; Ladha, J. K. Management of Biological Nitrogen Fixation for the Development of More Productive and Sustainable Agricultural Systems https://doi.org/10.1007/978-94-011-0055-7_1	book	January 1995
LinkImpute: Fast and Accurate Genotype Imputation for Nonmodel Organisms Money, Daniel; Gardner, Kyle; Migicovsky, Zoë G3: Genes\|Genomes\|Genetics, Vol. 5, Issue 11 https://doi.org/10.1534/g3.115.021667	journal	September 2015
Evolutionary Dynamics of Cereal Domestication de Wet, J. M. J. Bulletin of the Torrey Botanical Club, Vol. 102, Issue 6 https://doi.org/10.2307/2484756	journal	November 1975
Greenhouse gas emissions from global production and use of nitrogen synthetic fertilisers in agriculture Menegat, Stefano; Ledo, Alicia; Tirado, Reyes Scientific Reports, Vol. 12, Issue 1 https://doi.org/10.1038/s41598-022-18773-w	journal	August 2022
Mechanism of Molybdenum Nitrogenase Burgess, Barbara K.; Lowe, David J. Chemical Reviews, Vol. 96, Issue 7 https://doi.org/10.1021/cr950055x	journal	January 1996
SHOU4 Proteins Regulate Trafficking of Cellulose Synthase Complexes to the Plasma Membrane Polko, Joanna K.; Barnes, William J.; Voiniciuc, Cătălin Current Biology, Vol. 28, Issue 19 https://doi.org/10.1016/j.cub.2018.07.076	journal	October 2018
Two different novel cis -acting elements of erd1 , a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence Simpson, Sean D.; Nakashima, Kazuo; Narusaka, Yoshihiro The Plant Journal, Vol. 33, Issue 2 https://doi.org/10.1046/J.1365-313X.2003.01624.X	journal	January 2003
Effects of Combined Low Glutathione with Mild Oxidative and Low Phosphorus Stress on the Metabolism of Arabidopsis thaliana Fukushima, Atsushi; Iwasa, Mami; Nakabayashi, Ryo Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.01464	journal	August 2017
Sorghum Domestication and Diversification: A Current Archaeobotanical Perspective Fuller, Dorian Q.; Stevens, Chris J. Plants and People in the African Past https://doi.org/10.1007/978-3-319-89839-1_19	book	January 2018
The Sorghum bicolor reference genome: improved assembly, gene annotations, a transcriptome atlas, and signatures of genome organization McCormick, Ryan F.; Truong, Sandra K.; Sreedasyam, Avinash The Plant Journal, Vol. 93, Issue 2 https://doi.org/10.1111/TPJ.13781	journal	December 2017
Crop Prospects and Food Situation #1, March 2023 https://doi.org/10.4060/cc4665en	book	March 2023
The histone deacetylase OsHDAC1 epigenetically regulates the OsNAC6 gene that controls seedling root growth in rice Chung, Pil Joong; Kim, Yeon Shic; Jeong, Jin Seo The Plant Journal, Vol. 59, Issue 5 https://doi.org/10.1111/j.1365-313X.2009.03908.x	journal	August 2009
ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis Signora, Laurent; De Smet, Ive; Foyer, Christine H. The Plant Journal, Vol. 28, Issue 6 https://doi.org/10.1046/J.1365-313X.2001.01185.X	journal	December 2001
Controlling Dehiscence with Plastic Bags for Hand Crosses in Sorghum1 Schertz, K. F.; Clark, L. E. Crop Science, Vol. 7, Issue 5 https://doi.org/10.2135/cropsci1967.0011183X000700050040x	journal	January 1967
Genetic Control of Photoperiod Sensitivity in Maize Revealed by Joint Multiple Population Analysis Coles, Nathan D.; McMullen, Michael D.; Balint-Kurti, Peter J. Genetics, Vol. 184, Issue 3 https://doi.org/10.1534/genetics.109.110304	journal	December 2009
Population genomic and genome-wide association studies of agroclimatic traits in sorghum Morris, G. P.; Ramu, P.; Deshpande, S. P. Proceedings of the National Academy of Sciences, Vol. 110, Issue 2 https://doi.org/10.1073/PNAS.1215985110	journal	December 2012
Soil Acidification from Long-Term Use of Nitrogen Fertilizers on Winter Wheat Schroder, Jackie L.; Zhang, Hailin; Girma, Kefyalew Soil Science Society of America Journal, Vol. 75, Issue 3 https://doi.org/10.2136/sssaj2010.0187	journal	May 2011
Characterization of novel glycosyl hydrolases discovered by cell wall glycan directed monoclonal antibody screening and metagenome analysis of maize aerial root mucilage Pozzo, Tania; Higdon, Shawn M.; Pattathil, Sivakumar PLOS ONE, Vol. 13, Issue 9 https://doi.org/10.1371/JOURNAL.PONE.0204525	journal	September 2018
Mucilage secretion by aerial roots in sorghum (Sorghum bicolor): sugar profile, genetic diversity, GWAS and transcriptomic analysis Xu, Si; Li, Xiu-Qing; Guo, Hong Plant Molecular Biology, Vol. 112, Issue 6 https://doi.org/10.1007/s11103-023-01365-1	journal	June 2023
Plant cis-acting regulatory DNA elements (PLACE) database: 1999 Higo, K.; Ugawa, Y.; Iwamoto, M. Nucleic Acids Research, Vol. 27, Issue 1 https://doi.org/10.1093/NAR/27.1.297	journal	January 1999
Enhanced maize productivity by inoculation with diazotrophic bacteria Riggs, Patrick J.; Chelius, Marisa K.; Iniguez, A. Leonardo Functional Plant Biology, Vol. 28, Issue 9 https://doi.org/10.1071/PP01045	journal	January 2001
A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription Hobo, Tokunori; Kowyama, Yasuo; Hattori, Tsukaho Proceedings of the National Academy of Sciences, Vol. 96, Issue 26 https://doi.org/10.1073/pnas.96.26.15348	journal	December 1999
Development of Genome-wide Simple Sequence Repeat Markers Using Whole-genome Shotgun Sequences of Sorghum (Sorghum bicolor (L.) Moench) Yonemaru, J. -i.; Ando, T.; Mizubayashi, T. DNA Research, Vol. 16, Issue 3 https://doi.org/10.1093/DNARES/DSP005	journal	April 2009
S-nitrosylation triggers ABI5 degradation to promote seed germination and seedling growth Albertos, Pablo; Romero-Puertas, María C.; Tatematsu, Kiyoshi Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9669	journal	October 2015
DNA methylation and gene expression regulation associated with vascularization in Sorghum bicolor Turco, Gina M.; Kajala, Kaisa; Kunde‐Ramamoorthy, Govindarajan New Phytologist, Vol. 214, Issue 3 https://doi.org/10.1111/nph.14448	journal	February 2017
Nitrogen fixation and mucilage production on maize aerial roots is controlled by aerial root development and border cell functions Pankievicz, Vânia Carla Silva; Delaux, Pierre-Marc; Infante, Valentina Frontiers in Plant Science, Vol. 13 https://doi.org/10.3389/fpls.2022.977056	journal	October 2022
MEGA11: Molecular Evolutionary Genetics Analysis Version 11 Tamura, Koichiro; Stecher, Glen; Kumar, Sudhir Molecular Biology and Evolution, Vol. 38, Issue 7 https://doi.org/10.1093/molbev/msab120	journal	April 2021
Abscisic acid dynamics, signaling, and functions in plants Chen, Kong; Li, Guo‐Jun; Bressan, Ray A. Journal of Integrative Plant Biology, Vol. 62, Issue 1 https://doi.org/10.1111/JIPB.12899	journal	January 2020
Community Resources and Strategies for Association Mapping in Sorghum Casa, Alexandra M.; Pressoir, Gael; Brown, Patrick J. Crop Science, Vol. 48, Issue 1 https://doi.org/10.2135/cropsci2007.02.0080	journal	January 2008
Shrinkage Estimation of the Realized Relationship Matrix Endelman, Jeffrey B.; Jannink, Jean-Luc G3: Genes\|Genomes\|Genetics, Vol. 2, Issue 11 https://doi.org/10.1534/g3.112.004259	journal	November 2012
Developing a Mini Core Collection of Sorghum for Diversified Utilization of Germplasm Upadhyaya, H. D.; Pundir, R. P. S.; Dwivedi, S. L. Crop Science, Vol. 49, Issue 5 https://doi.org/10.2135/CROPSCI2009.01.0014	journal	January 2009
Loss of an MDR Transporter in Compact Stalks of Maize br2 and Sorghum dw3 Mutants Multani, D. S. Science, Vol. 302, Issue 5642 https://doi.org/10.1126/science.1086072	journal	October 2003
Expanding and Vetting Gene Annotations through Transcriptome and Methylome Sequencing Olson, Andrew; Klein, Robert R.; Dugas, Diana V. The Plant Genome, Vol. 7, Issue 2 https://doi.org/10.3835/PLANTGENOME2013.08.0025	journal	January 2014
Evaluation of nitrogen isotopes as indicators of nitrate contamination sources in an agricultural watershed Kellman, L. M.; Hillaire-Marcel, C. Agriculture, Ecosystems & Environment, Vol. 95, Issue 1 https://doi.org/10.1016/S0167-8809(02)00168-8	journal	April 2003
A N ₂ -fixing endophytic Burkholderia sp. associated with maize plants cultivated in Mexico Estrada, Paulina; Mavingui, Patrick; Cournoyer, Benoit Canadian Journal of Microbiology, Vol. 48, Issue 4 https://doi.org/10.1139/w02-023	journal	April 2002
Potential for ethanol production from different sorghum cultivars Castro, Eulogio; Nieves, Ismael U.; Rondón, Vanessa Industrial Crops and Products, Vol. 109 https://doi.org/10.1016/J.INDCROP.2017.08.050	journal	December 2017
The Sorghum bicolor genome and the diversification of grasses Paterson, Andrew H.; Bowers, John E.; Bruggmann, Rémy Nature, Vol. 457, Issue 7229 https://doi.org/10.1038/nature07723	journal	January 2009
Mapping quantitative trait loci associated with days to flowering and photoperiod sensitivity in rice (Oryza sativa L.) Maheswaran, M.; Huang, Ning; Sreerangasamy, S. R. Molecular Breeding, Vol. 6, Issue 2, p. 145-155 https://doi.org/10.1023/A:1009618621720	journal	April 2000
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
The genetic architecture of nodal root number in maize Zhang, Zhihai; Zhang, Xuan; Lin, Zhelong The Plant Journal, Vol. 93, Issue 6 https://doi.org/10.1111/TPJ.13828	journal	February 2018
Confidence Intervals for the Means of Dependent, Normally Distributed Variables Dunn, Olive Jean Journal of the American Statistical Association, Vol. 54, Issue 287 https://doi.org/10.1080/01621459.1959.10501524	journal	September 1959
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing Benjamini, Yoav; Hochberg, Yosef Journal of the Royal Statistical Society: Series B (Methodological), Vol. 57, Issue 1 https://doi.org/10.1111/j.2517-6161.1995.tb02031.x	journal	January 1995
Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Aida, M.; Ishida, T.; Fukaki, H. The Plant Cell, Vol. 9, Issue 6 https://doi.org/10.1105/TPC.9.6.841	journal	June 1997
Inference of Population Structure Using Multilocus Genotype Data Pritchard, Jonathan K.; Stephens, Matthew; Donnelly, Peter Genetics, Vol. 155, Issue 2 https://doi.org/10.1093/genetics/155.2.945	journal	June 2000
A conserved proline residue in the leucine zipper region of AtbZIP34 and AtbZIP61 in Arabidopsis thaliana interferes with the formation of homodimer Shen, Huaishun; Cao, Kaiming; Wang, Xiping Biochemical and Biophysical Research Communications, Vol. 362, Issue 2 https://doi.org/10.1016/j.bbrc.2007.08.026	journal	October 2007
The Road to Sorghum Domestication: Evidence From Nucleotide Diversity and Gene Expression Patterns Burgarella, Concetta; Berger, Angélique; Glémin, Sylvain Frontiers in Plant Science, Vol. 12 https://doi.org/10.3389/fpls.2021.666075	journal	August 2021
An Integrated Genotyping‐by‐Sequencing Polymorphism Map for Over 10,000 Sorghum Genotypes Hu, Zhenbin; Olatoye, Marcus O.; Marla, Sandeep The Plant Genome, Vol. 12, Issue 1 https://doi.org/10.3835/PLANTGENOME2018.06.0044	journal	March 2019
The Arabidopsis bZIP transcription factor family — an update Dröge-Laser, Wolfgang; Snoek, Basten L.; Snel, Berend Current Opinion in Plant Biology, Vol. 45 https://doi.org/10.1016/j.pbi.2018.05.001	journal	October 2018
Sorghum Dw1, an agronomically important gene for lodging resistance, encodes a novel protein involved in cell proliferation Yamaguchi, Miki; Fujimoto, Haruka; Hirano, Ko Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep28366	journal	June 2016
Impact of climate change on agriculture production and its sustainable solutions Arora, Naveen Kumar Environmental Sustainability, Vol. 2, Issue 2 https://doi.org/10.1007/s42398-019-00078-w	journal	June 2019
Genetic Structure and Linkage Disequilibrium in a Diverse, Representative Collection of the C4 Model Plant, Sorghum bicolor Wang, Yi-Hong; Upadhyaya, Hari D.; Burrell, A. Millie G3 Genes\|Genomes\|Genetics, Vol. 3, Issue 5 https://doi.org/10.1534/g3.112.004861	journal	May 2013
Abscisic Acid–Induced Transcription Is Mediated by Phosphorylation of an Abscisic Acid Response Element Binding Factor, TRAB1 Kagaya, Yasuaki; Hobo, Tokunori; Murata, Michiharu The Plant Cell, Vol. 14, Issue 12 https://doi.org/10.1105/tpc.005272	journal	November 2002
Strategy for Structural Elucidation of Polysaccharides: Elucidation of a Maize Mucilage that Harbors Diazotrophic Bacteria Amicucci, Matthew J.; Galermo, Ace G.; Guerrero, Andres Analytical Chemistry, Vol. 91, Issue 11 https://doi.org/10.1021/ACS.ANALCHEM.9B00789	journal	April 2019
Jasmonate biosynthesis arising from altered cell walls is prompted by turgor-driven mechanical compression Mielke, Stefan; Zimmer, Marlene; Meena, Mukesh Kumar Science Advances, Vol. 7, Issue 7 https://doi.org/10.1126/sciadv.abf0356	journal	February 2021
DET1, a negative regulator of light-mediated development and gene expression in arabidopsis, encodes a novel nuclear-localized protein Pepper, Alan; Delaney, Terrence; Washburnt, Tracy Cell, Vol. 78, Issue 1 https://doi.org/10.1016/0092-8674(94)90577-0	journal	July 1994
Close Split of Sorghum and Maize Genome Progenitors Swigonova, Z. Genome Research, Vol. 14, Issue 10a https://doi.org/10.1101/gr.2332504	journal	September 2004
Mixed linear model approach adapted for genome-wide association studies Zhang, Zhiwu; Ersoz, Elhan; Lai, Chao-Qiang Nature Genetics, Vol. 42, Issue 4 https://doi.org/10.1038/ng.546	journal	March 2010
Transcriptional activation by Arabidopsis GT‐1 may be through interaction with TFIIA–TBP–TATA complex Le Gourrierec, José; Li, You‐Fang; Zhou, Dao‐Xiu The Plant Journal, Vol. 18, Issue 6 https://doi.org/10.1046/J.1365-313X.1999.00482.X	journal	June 1999
Hidden Branches: Developments in Root System Architecture Osmont, Karen S.; Sibout, Richard; Hardtke, Christian S. Annual Review of Plant Biology, Vol. 58, Issue 1 https://doi.org/10.1146/annurev.arplant.58.032806.104006	journal	June 2007
Nitrogen fixation in a landrace of maize is supported by a mucilage-associated diazotrophic microbiota Van Deynze, Allen; Zamora, Pablo; Delaux, Pierre-Marc PLOS Biology, Vol. 16, Issue 8 https://doi.org/10.1371/JOURNAL.PBIO.2006352	journal	August 2018
Colonization of wheat (Triticum vulgare L.) by N₂‐fixing cyanobacteria: II. An ultrastructural study Gantar, M.; Kerby, N. W.; Rowell, P. New Phytologist, Vol. 118, Issue 3 https://doi.org/10.1111/j.1469-8137.1991.tb00031.x	journal	July 1991
AtNAP, a NAC family transcription factor, has an important role in leaf senescence Guo, Yongfeng; Gan, Susheng The Plant Journal, Vol. 46, Issue 4, p. 601-612 https://doi.org/10.1111/J.1365-313X.2006.02723.X	journal	May 2006
Intentional versus unintentional nitrogen use in the United States: trends, efficiency and implications Houlton, Benjamin Z.; Boyer, Elizabeth; Finzi, Adrien Biogeochemistry, Vol. 114, Issue 1-3 https://doi.org/10.1007/s10533-012-9801-5	journal	October 2012
Gene Regulatory Network of Secondary Cell Wall Biosynthesis during VND7 Induced de novo Xylem Formation Tong, Haonan; Chen, Hao International Journal of Bioscience, Biochemistry and Bioinformatics, Vol. 11, Issue 4 https://doi.org/10.17706/ijbbb.2021.11.4.74-81	journal	October 2021
Transcription Factors in Rice: A Genome-wide Comparative Analysis between Monocots and Eudicots Xiong, Yuqing; Liu, Tieyan; Tian, Chaoguang Plant Molecular Biology, Vol. 59, Issue 1 https://doi.org/10.1007/S11103-005-6503-6	journal	September 2005
Physiological and Genetic Changes of Irrigated Wheat in the Post–Green Revolution Period and Approaches for Meeting Projected Global Demand Reynolds, M. P.; Rajaram, S.; Sayre, K. D. Crop Science, Vol. 39, Issue 6 https://doi.org/10.2135/cropsci1999.3961611x	journal	November 1999
A nitrogen fixing symbiosis-specific pathway required for legume flowering Yun, Jinxia; Wang, Can; Zhang, Fengrong Science Advances, Vol. 9, Issue 2 https://doi.org/10.1126/sciadv.ade1150	journal	January 2023
Analysis of polysaccharides and monosaccharides in the root mucilage of maize (Zea mays L.) by gas chromatography Osborn, Helen M. I.; Lochey, Franck; Mosley, Lydia Journal of Chromatography A, Vol. 831, Issue 2 https://doi.org/10.1016/S0021-9673(98)00935-2	journal	January 1999
Harvest index: a review of its use in plant breeding and crop physiology Hay, R. K. M. Annals of Applied Biology, Vol. 126, Issue 1 https://doi.org/10.1111/j.1744-7348.1995.tb05015.x	journal	February 1995
OrthoDB v11: annotation of orthologs in the widest sampling of organismal diversity Kuznetsov, Dmitry; Tegenfeldt, Fredrik; Manni, Mosè Nucleic Acids Research, Vol. 51, Issue D1 https://doi.org/10.1093/NAR/GKAC998	journal	November 2022
The ABRE-binding bZIP transcription factor OsABF2 is a positive regulator of abiotic stress and ABA signaling in rice Hossain, Md. Amir; Cho, Jung-Il; Han, Muho Journal of Plant Physiology, Vol. 167, Issue 17 https://doi.org/10.1016/j.jplph.2010.05.008	journal	November 2010
A unified mixed-model method for association mapping that accounts for multiple levels of relatedness Yu, Jianming; Pressoir, Gael; Briggs, William H. Nature Genetics, Vol. 38, Issue 2 https://doi.org/10.1038/ng1702	journal	December 2005
Expression Atlas update: gene and protein expression in multiple species Moreno, Pablo; Fexova, Silvie; George, Nancy Nucleic Acids Research, Vol. 50, Issue D1 https://doi.org/10.1093/nar/gkab1030	journal	November 2021
Rice transcription factor OsMADS25 modulates root growth and confers salinity tolerance via the ABA–mediated regulatory pathway and ROS scavenging Xu, Ning; Chu, Yanli; Chen, Hongli PLOS Genetics, Vol. 14, Issue 10 https://doi.org/10.1371/JOURNAL.PGEN.1007662	journal	October 2018
The Arabidopsis Abscisic Acid Response Gene ABI5 Encodes a Basic Leucine Zipper Transcription Factor Finkelstein, Ruth R.; Lynch, Tim J. The Plant Cell, Vol. 12, Issue 4 https://doi.org/10.1105/tpc.12.4.599	journal	April 2000
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
The No Apical Meristem Gene of Petunia Is Required for Pattern Formation in Embryos and Flowers and Is Expressed at Meristem and Primordia Boundaries Souer, Erik; van Houwelingen, Adèle; Kloos, Daisy Cell, Vol. 85, Issue 2 https://doi.org/10.1016/S0092-8674(00)81093-4	journal	April 1996
Molecular characterization of AtNAM: a member of the Arabidopsis NAC domain superfamily Duval, Manuel; Hsieh, Tzung-Fu; Kim, Soo Young Plant Molecular Biology, Vol. 50, Issue 2, p. 237-248 https://doi.org/10.1023/A:1016028530943	journal	September 2002
Dissecting Arabidopsis lateral root development Casimiro, Ilda; Beeckman, Tom; Graham, Neil Trends in Plant Science, Vol. 8, Issue 4 https://doi.org/10.1016/S1360-1385(03)00051-7	journal	April 2003
Negative regulatory roles of DE-ETIOLATED1 in flowering time inArabidopsis Kang, Min-Young; Yoo, Soo-Cheul; Kwon, Hye-Young Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep09728	journal	May 2015
Azoarcus Grass Endophytes Contribute Fixed Nitrogen to the Plant in an Unculturable State Hurek, Thomas; Handley, Linda L.; Reinhold-Hurek, Barbara Molecular Plant-Microbe Interactions, Vol. 15, Issue 3 https://doi.org/10.1094/MPMI.2002.15.3.233	journal	March 2002
Complete genome sequence of the sugarcane nitrogen-fixing endophyte Gluconacetobacter diazotrophicus Pal5 Bertalan, Marcelo; Albano, Rodolpho; de Pádua, Vânia BMC Genomics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2164-10-450	journal	January 2009
ABD1 Is anArabidopsisDCAF Substrate Receptor for CUL4-DDB1–Based E3 Ligases That Acts as a Negative Regulator of Abscisic Acid Signaling Seo, Kyoung-In; Lee, Jae-Hoon; Nezames, Cynthia D. The Plant Cell, Vol. 26, Issue 2 https://doi.org/10.1105/tpc.113.119974	journal	February 2014
A Null Mutation in a bZIP Factor Confers ABA-Insensitivity in Arabidopsis thaliana Lopez-Molina, L.; Chua, N. -H. Plant and Cell Physiology, Vol. 41, Issue 5 https://doi.org/10.1093/pcp/41.5.541	journal	May 2000
Abscisic acid facilitates phosphate acquisition through the transcription factor ABA INSENSITIVE5 in Arabidopsis Zhang, Yu; Li, Ting‐Ting; Wang, Lin‐Feng The Plant Journal, Vol. 111, Issue 1 https://doi.org/10.1111/TPJ.15791	journal	May 2022
Molecular mapping of the brace root traits in sorghum (Sorghum bicolor L. Moench) Li, Ronggai; Han, Yucui; Lv, Peng Breeding Science, Vol. 64, Issue 2 https://doi.org/10.1270/JSBBS.64.193	journal	January 2014

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