Integration of multi-omics data reveals interplay between brassinosteroid and Target of Rapamycin Complex signaling in Arabidopsis

Authors: MONTES, CHRISTIAN - Iowa State University; WANG, PING - Iowa State University; LIAO, CHING-YI - Iowa State University; NOLAN, TREVOR - Iowa State University; SONG, GAOYUAN - Iowa State University; CLARK, NATALIE - Iowa State University; Elmore, James - Mitch; GUO, HONGQING - Iowa State University; BASSHAM, DIANE - Iowa State University; YIN, YANHAI - Iowa State University; WALLEY, JUSTIN - Iowa State University

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/16/2022
Publication Date: 10/6/2022
Citation: Montes, C.M., Wang, P., Liao, C., Nolan, T.M., Song, G., Clark, N.M., Elmore, J.M., Guo, H., Bassham, D.C., Yin, Y., Walley, J.W. 2022. Integration of multi-omics data reveals interplay between brassinosteroid and Target of Rapamycin Complex signaling in Arabidopsis. New Phytologist. 236(3):893–910. https://doi.org/10.1111/nph.18404.
DOI: https://doi.org/10.1111/nph.18404

Interpretive Summary: Throughout their lifecycle, plants must grow and respond to diverse environmental stresses. These responses are coordinated via hormones and complex signaling networks that alter gene expression. Brassinosteroid (BR) hormone signaling and the Target of Rapamycin Complex (TORC) have emerged as two key pathways coordinating growth and stress outcomes. However, the connection and molecular interplay between these two pathways is poorly understood. To gain a global view of BR and TORC crosstalk, we performed deep molecular profiling to quantify the RNA, protein, and phosphorylated protein content of genetic mutants with altered BR and TORC activity. Using this wealth of information, we reconstructed an integrated signaling network that predicts how gene expression is regulated. We used this integrated network to identify novel genes whose mutant lines showed either altered growth in response to BR and/or levels of autophagy, a cellular recycling process that occurs during stress responses. Our results provide a robust road map of how BR and TORC pathways crosstalk at system-wide levels. Together, these studies further our understanding of the dynamic interplay between BR and TORC signaling.

Technical Abstract: Brassinosteroids (BR) and Target of Rapamycin Complex (TORC) are two major actors coordinating plant growth and stress responses. BRs function through a signaling pathway to extensively regulate gene expression and TORC is known to regulate translation and autophagy. Recent studies revealed crosstalk between these two pathways, but a system-wide view of their interplay is still missing. Thus, we quantified the level of 23,181 transcripts, 11,238 proteins, and 27,886 phosphorylation sites in wild-type Arabidopsis as well as mutants with altered levels of either BIN2 or RAPTOR1B, two key players in BR and TORC signaling, respectively. We found that perturbation of BIN2 or RAPTOR1B levels affects a common set of gene-products involved in growth and stress responses. Furthermore, we used the multi-omic data to reconstruct an integrated signaling network. We screened 42 candidate genes identified from the integrated network and found that loss of function mutants of many of these proteins led to an altered BR response and/or modulated autophagy activity. Altogether, these results establish a predictive network that defines the molecular interactions of BR and TORC in the regulation of plant growth/stress balance.