Traceback of core transcription factors for soybean root growth maintenance under water deficit

Authors: LIN, LI - University Of Missouri; VELDE, JAN VAN DE - Ghent University; NGUYEN, NA - University Of Missouri; Meyer, Ricky - Rick; An, Yong-Qiang - Charles; SONG, LI - University Of Missouri; VALLIYODAN, BABU - University Of Missouri; PRINCE, SILVAS - University Of Missouri; WAN, JINRONG - University Of Missouri; MURPHY, MACKENSIE - University Of Missouri; KIM, EIRU - Yonsei University; LEE, INSUK - Yonsei University; PENTECOST, GENEVIEVE - University Of Missouri; ZHU, CHENGSONG - University Of Missouri; KUSHWAHA, GARIMA - University Of Missouri; JOSHI, TRUPTI - University Of Missouri; CHEN, WEI - University Of Missouri; PATIL, GUNVANT - University Of Missouri; MUTAVA, RAYMOND - University Of Missouri; XU, DONG - University Of Missouri; VANDEPOELE, KLAAS - University Of Missouri; NGUYEN, HENRY - University Of Missouri

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/20/2020
Publication Date: 3/20/2020
Citation: Lin, L., Velde, J., Nguyen, N., Meyer, R.J., An, Y., Song, L., Valliyodan, B., Prince, S., Wan, J., Murphy, M., Kim, E., Lee, I., Pentecost, G., Zhu, C., Kushwaha, G., Joshi, T., Chen, W., Patil, G., Mutava, R., Xu, D., Vandepoele, K., Nguyen, H.T. 2020. Network-assisted prioritization of transcription factors involved in root growth maintenance under water deficits in soybean. The Plant Cell. Article 2020.03.19.999482. https://doi.org/10.1101/2020.03.19.999482.
DOI: https://doi.org/10.1101/2020.03.19.999482

Interpretive Summary: Maintaining root growth in water-deficient soils is one of the more important biological processes for soybean agricultural production. It is accomplished through the concerted activities of many genes operating in interrelated networks. Illustrating these networks and identifying the key regulatory genes within them is crucial for designing genetic strategies to develop drought tolerant soybeans. In this study, we developed an informatic platform that integrated large-scale gene expression analyses, a variety of data mining strategies, and laboratory based experimental data to generate a useful gene network model. We further applied the informatics platform to infer a core set of gene networks and experimentally validated several of the key regulatory genes within the networks. We demonstrated that two genes that respond to water deficit stress (GmBEE and GmABF) likely function through mediating signal pathways of two phytohormones, brassinosteroids (BR) and abscisic acid (ABA). The genes and networks that we illustrate and validated experimentally can progress into breeding strategies for the genetic improvement of soybean drought tolerance. This informatics platform will also be useful to illustrate genes and networks for other agronomic traits.

Technical Abstract: Some crops inhibit shoot growth but maintain root growth under water-deficit conditions. Unraveling the molecular mechanisms of root plasticity under water deficit conditions in plants remains a major challenge. We developed an efficient platform for identifying core transcription factors (TFs) that collectively regulate each other and/or themselves in response to water stress, and exploring their interconnected regulatory circuitry involved in root growth maintenance under water deficit in soybean. We performed multi-species phylogenetic footprinting combined with spatial-temporal transcriptome analysis of soybean (Glycine max) roots under water deficit to identify conserved motifs that function in the water-stress response. Using these functional conserved cis-motifs, we applied a new approach to trace back motifs-associated core TFs ingroup as signal mediators, which mediate signaling between abiotic and endogenous stimuli. We integrated a co-functional TF–TF network and conserved motif-centered TF–DNA networks to construct a core TF network defined by mutual cross-regulation among core TFs. We found that core TF ARG (Abscisic acid response element binding factor-like Root Growth regulator) represses BRG (Brassinosteroid enhanced expression-like Root Growth regulator) expression through binding to its promoter at a conserved binding site. ARG and BRG antagonistically regulate Phytochrome-interacting factor-like Root Growth regulator (PRG) and combinatorially regulate some other core TFs. These core TFs form complex regulatory circuits to integrate light and multiple hormone signaling pathways and maintain root growth in response to varying degrees of water stress. Our study provides valuable information to unravel the complicated mechanisms of molecular networks involved in the regulation of root growth under water deficit.