Insights into soybean transcriptome reconfiguration under hypoxic stress: Functional, regulatory, structural, and compositional characterization

Authors: NAKAYAMA, THIAGO - Universidade Federal De Vicosa; RODRIGUES, FABIANA - Embrapa; NEUMAIER, NORMAN - Embrapa; MARCOLINA-GOMES, JULIANA - Embrapa; MOLINARI, HUGO - Embrapa; SANTIAGO, THAIS - Embrapa; FORMIGHIERI, EDUARDO - Embrapa; BASSO, MARCOS - Embrapa; FARIAS, JOSE - Embrapa; EMYGDIO, BEATRIZ - Embrapa; DE OLIVEIRA, ANA - Embrapa; CAMPOS, ANGELA - Embrapa; BOREM, ALUIZIO - Universidade Federal De Vicosa; Harmon, Frank; MERTZ-HENNING, LILIANE - Embrapa; NEPOMUCENO, ALEXANDRE - Embrapa

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/27/2017
Publication Date: 11/18/2017
Citation: Nakayama, T.J., Rodrigues, F.A., Neumaier, N., Marcolina-Gomes, J., Molinari, H.B., Santiago, T.R., Formighieri, E.F., Basso, M.F., Farias, J.R., Emygdio, B.M., De Oliveira, A.C., Campos, A.D., Borem, A., Coleman-Derr, D.A., Mertz-Henning, L.M., Nepomuceno, A. 2017. Insights into soybean transcriptome reconfiguration under hypoxic stress: Functional, regulatory, structural, and compositional characterization. PLoS One. 12(11):e0187920. https://doi.org/10.1371/journal.pone.0187920.
DOI: https://doi.org/10.1371/journal.pone.0187920

Interpretive Summary: Flooding negatively impacts current production of soybean (Glycine max), as well as expansion of its cultivation. A primary effect of flooding in affected plant tissues, like root, is oxygen deficiency, known as hypoxia, that interferes with energy production in plant cells. Extended episodes of hypoxic stress result in cell, tissue, and plant death. This study analyzed gene expression mechanisms used by soybean plants to cope with hypoxic stress by identifying differences in gene expression between a flood-tolerant soybean variety, Embrapa 45, and flood-sensitive soybean variety, BR 4. This analysis discovered substantial differences in global gene regulation between Embrapa 45 and BR4, as well as specific changes in regulation of hypoxia response-related genes. To understand potential mechanistic causes for the differences in gene expression, the authors contrasted gene structure between the two varieties. This study found genes with different expression between varieties had different regulatory sequence composition upstream of these genes, including stress-associated regulatory elements known as ABRE elements. Additional data confirms that local-acting ABRE elements participate in hypoxia-mediated gene expression in soybean roots. Overall, this study highlights important regulatory mechanisms associated soybean response to flooding and how the plant has developed tolerance to this stress.

Technical Abstract: Soybean (Glycine max) is one of the major crops worldwide and flooding stress affects the production and expansion of cultivated areas. Oxygen is essential for mitochondrial aerobic respiration to supply the energy demand of plant cells. Because oxygen diffusion in water is 10,000 times lower than in air, partial (hypoxic) or total (anoxic) oxygen deficiency is important component of flooding. Even when oxygen is externally available, oxygen deficiency frequently occurs in bulky, dense or metabolically active tissues such as phloem, meristems, seeds, and fruits. In this study, we analyzed conserved and divergent root transcriptional responses between flood-tolerant Embrapa 45 and flood-sensitive BR 4 soybean cultivars under hypoxic stress conditions with RNA-seq. To understand how soybean genes evolve and respond to hypoxia, stable and differentially expressed genes were characterized structurally and compositionally comparing its mechanistic relationship. Between cultivars, Embrapa 45 showed less up- and more down-regulated genes, and stronger induction of phosphoglucomutase (Glyma05g34790), unknown protein related to N-terminal protein myristoylation (Glyma06g03430), protein suppressor of phyA-105 (Glyma06g37080), and fibrillin (Glyma10g32620). RNA-seq and qRT-PCR analysis of non-symbiotic hemoglobin (Glyma11g12980) indicated divergence in gene structure between cultivars. Transcriptional changes for genes in amino acids and derivative metabolic process suggest involvement of amino acids metabolism in tRNA modifications, translation accuracy/efficiency, and endoplasmic reticulum stress in both cultivars under hypoxia. Gene groups differed in promoter TATA box, ABREs (ABA-responsive elements), and CRT/DREs (C-repeat/dehydration-responsive elements) frequency. Gene groups also differed in structure, composition, and codon usage, indicating biological significances. Additional data suggests that cis-acting ABRE elements can mediate gene expression independent of ABA in soybean roots under hypoxia.