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Integrated omics networks reveal the temporal signaling events of brassinosteroid response in Arabidopsis

Author

Listed:
  • Natalie M. Clark

    (Iowa State University)

  • Trevor M. Nolan

    (Iowa State University
    Duke University)

  • Ping Wang

    (Iowa State University)

  • Gaoyuan Song

    (Iowa State University)

  • Christian Montes

    (Iowa State University)

  • Conner T. Valentine

    (Iowa State University)

  • Hongqing Guo

    (Iowa State University)

  • Rosangela Sozzani

    (North Carolina State University)

  • Yanhai Yin

    (Iowa State University)

  • Justin W. Walley

    (Iowa State University)

Abstract

Brassinosteroids (BRs) are plant steroid hormones that regulate cell division and stress response. Here we use a systems biology approach to integrate multi-omic datasets and unravel the molecular signaling events of BR response in Arabidopsis. We profile the levels of 26,669 transcripts, 9,533 protein groups, and 26,617 phosphorylation sites from Arabidopsis seedlings treated with brassinolide (BL) for six different lengths of time. We then construct a network inference pipeline called Spatiotemporal Clustering and Inference of Omics Networks (SC-ION) to integrate these data. We use our network predictions to identify putative phosphorylation sites on BES1 and experimentally validate their importance. Additionally, we identify BRONTOSAURUS (BRON) as a transcription factor that regulates cell division, and we show that BRON expression is modulated by BR-responsive kinases and transcription factors. This work demonstrates the power of integrative network analysis applied to multi-omic data and provides fundamental insights into the molecular signaling events occurring during BR response.

Suggested Citation

  • Natalie M. Clark & Trevor M. Nolan & Ping Wang & Gaoyuan Song & Christian Montes & Conner T. Valentine & Hongqing Guo & Rosangela Sozzani & Yanhai Yin & Justin W. Walley, 2021. "Integrated omics networks reveal the temporal signaling events of brassinosteroid response in Arabidopsis," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26165-3
    DOI: 10.1038/s41467-021-26165-3
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    References listed on IDEAS

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    1. Vân Anh Huynh-Thu & Alexandre Irrthum & Louis Wehenkel & Pierre Geurts, 2010. "Inferring Regulatory Networks from Expression Data Using Tree-Based Methods," PLOS ONE, Public Library of Science, vol. 5(9), pages 1-10, September.
    2. Giorgino, Toni, 2009. "Computing and Visualizing Dynamic Time Warping Alignments in R: The dtw Package," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 31(i07).
    3. Moysés Nascimento & Fabyano Fonseca e Silva & Thelma Sáfadi & Ana Carolina Campana Nascimento & Talles Eduardo Maciel Ferreira & Laís Mayara Azevedo Barroso & Camila Ferreira Azevedo & Simone Eliza Fa, 2017. "Independent Component Analysis (ICA) based-clustering of temporal RNA-seq data," PLOS ONE, Public Library of Science, vol. 12(7), pages 1-12, July.
    4. Huaxun Ye & Sanzhen Liu & Buyun Tang & Jiani Chen & Zhouli Xie & Trevor M. Nolan & Hao Jiang & Hongqing Guo & Hung-Ying Lin & Lei Li & Yanqun Wang & Hongning Tong & Mingcai Zhang & Chengcai Chu & Zhao, 2017. "RD26 mediates crosstalk between drought and brassinosteroid signalling pathways," Nature Communications, Nature, vol. 8(1), pages 1-13, April.
    5. Natalie M. Clark & Eli Buckner & Adam P. Fisher & Emily C. Nelson & Thomas T. Nguyen & Abigail R. Simmons & Maria A. Luis Balaguer & Tiara Butler-Smith & Parnell J. Sheldon & Dominique C. Bergmann & C, 2019. "Stem-cell-ubiquitous genes spatiotemporally coordinate division through regulation of stem-cell-specific gene networks," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
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    Cited by:

    1. Teng Jing & Yuying Wu & Yanwen Yu & Jiankun Li & Xiaohuan Mu & Liping Xu & Xi Wang & Guang Qi & Jihua Tang & Daowen Wang & Shuhua Yang & Jian Hua & Mingyue Gou, 2024. "Copine proteins are required for brassinosteroid signaling in maize and Arabidopsis," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Xi Wang & Juan Li & Linqian Han & Chengyong Liang & Jiaxin Li & Xiaoyang Shang & Xinxin Miao & Zi Luo & Wanchao Zhu & Zhao Li & Tianhuan Li & Yongwen Qi & Huihui Li & Xiaoduo Lu & Lin Li, 2023. "QTG-Miner aids rapid dissection of the genetic base of tassel branch number in maize," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

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