Alex Borowsky

All Publications

• Rewiring gene circuitry for plant improvement NATURE GENETICS Borowsky, A. T., Bailey-Serres, J. 2024; 56 (8): 1574-1582

  Abstract

  Aspirations for high crop growth and yield, nutritional quality and bioproduction of materials are challenged by climate change and limited adoption of new technologies. Here, we review recent advances in approaches to profile and model gene regulatory activity over developmental and response time in specific cells, which have revealed the basis of variation in plant phenotypes: both redeployment of key regulators to new contexts and their repurposing to control different slates of genes. New synthetic biology tools allow tunable, spatiotemporal regulation of transgenes, while recent gene-editing technologies enable manipulation of the regulation of native genes. Ultimately, understanding how gene circuitry is wired to control form and function across varied plant species, combined with advanced technology to rewire that circuitry, will unlock solutions to our greatest challenges in agriculture, energy and the environment.

  View details for DOI 10.1038/s41588-024-01806-7

  View details for Web of Science ID 001279234100001

  View details for PubMedID 39075207

  View details for PubMedCentralID 7024682

• spatialHeatmap: visualizing spatial bulk and single-cell assays in anatomical images NAR GENOMICS AND BIOINFORMATICS Zhang, J., Zhang, L., Gongol, B., Hayes, J., Borowsky, A. T., Bailey-Serres, J., Girke, T. 2024; 6 (1): lqae006

  Abstract

  Visualizing spatial assay data in anatomical images is vital for understanding biological processes in cell, tissue, and organ organizations. Technologies requiring this functionality include traditional one-at-a-time assays, and bulk and single-cell omics experiments, including RNA-seq and proteomics. The spatialHeatmap software provides a series of powerful new methods for these needs, and allows users to work with adequately formatted anatomical images from public collections or custom images. It colors the spatial features (e.g. tissues) annotated in the images according to the measured or predicted abundance levels of biomolecules (e.g. mRNAs) using a color key. This core functionality of the package is called a spatial heatmap plot. Single-cell data can be co-visualized in composite plots that combine spatial heatmaps with embedding plots of high-dimensional data. The resulting spatial context information is essential for gaining insights into the tissue-level organization of single-cell data, or vice versa. Additional core functionalities include the automated identification of biomolecules with spatially selective abundance patterns and clusters of biomolecules sharing similar abundance profiles. To appeal to both non-expert and computational users, spatialHeatmap provides a graphical and a command-line interface, respectively. It is distributed as a free, open-source Bioconductor package (https://bioconductor.org/packages/spatialHeatmap) that users can install on personal computers, shared servers, or cloud systems.

  View details for DOI 10.1093/nargab/lqae006

  View details for Web of Science ID 001155382800003

  View details for PubMedID 38312938

  View details for PubMedCentralID PMC10836942

• A suberized exodermis is required for tomato drought tolerance NATURE PLANTS Canto-Pastor, A., Kajala, K., Shaar-Moshe, L., Manzano, C., Timilsena, P., De Bellis, D., Gray, S., Holbein, J., Yang, H., Mohammad, S., Nirmal, N., Suresh, K., Ursache, R., Mason, G., Gouran, M., West, D. A., Borowsky, A. T., Shackel, K. A., Sinha, N., Bailey-Serres, J., Geldner, N., Li, S., Franke, R., Brady, S. M. 2024; 10 (1): 118-+

  Abstract

  Plant roots integrate environmental signals with development using exquisite spatiotemporal control. This is apparent in the deposition of suberin, an apoplastic diffusion barrier, which regulates flow of water, solutes and gases, and is environmentally plastic. Suberin is considered a hallmark of endodermal differentiation but is absent in the tomato endodermis. Instead, suberin is present in the exodermis, a cell type that is absent in the model organism Arabidopsis thaliana. Here we demonstrate that the suberin regulatory network has the same parts driving suberin production in the tomato exodermis and the Arabidopsis endodermis. Despite this co-option of network components, the network has undergone rewiring to drive distinct spatial expression and with distinct contributions of specific genes. Functional genetic analyses of the tomato MYB92 transcription factor and ASFT enzyme demonstrate the importance of exodermal suberin for a plant water-deficit response and that the exodermal barrier serves an equivalent function to that of the endodermis and can act in its place.

  View details for DOI 10.1038/s41477-023-01567-x

  View details for Web of Science ID 001135121800004

  View details for PubMedID 38168610

  View details for PubMedCentralID PMC10808073

• Gene regulatory networks shape developmental plasticity of root cell types under water extremes in rice DEVELOPMENTAL CELL Reynoso, M. A., Borowsky, A. T., Pauluzzi, G. C., Yeung, E., Zhang, J., Formentin, E., Velasco, J., Cabanlit, S., Duvenjian, C., Prior, M. J., Akmakjian, G. Z., Deal, R. B., Sinha, N. R., Brady, S. M., Girke, T., Bailey-Serres, J. 2022; 57 (9): 1177-+

  Abstract

  Understanding how roots modulate development under varied irrigation or rainfall is crucial for development of climate-resilient crops. We established a toolbox of tagged rice lines to profile translating mRNAs and chromatin accessibility within specific cell populations. We used these to study roots in a range of environments: plates in the lab, controlled greenhouse stress and recovery conditions, and outdoors in a paddy. Integration of chromatin and mRNA data resolves regulatory networks of the following: cycle genes in proliferating cells that attenuate DNA synthesis under submergence; genes involved in auxin signaling, the circadian clock, and small RNA regulation in ground tissue; and suberin biosynthesis, iron transporters, and nitrogen assimilation in endodermal/exodermal cells modulated with water availability. By applying a systems approach, we identify known and candidate driver transcription factors of water-deficit responses and xylem development plasticity. Collectively, this resource will facilitate genetic improvements in root systems for optimal climate resilience.

  View details for DOI 10.1016/j.devcel.2022.04.013

  View details for Web of Science ID 000799181500001

  View details for PubMedID 35504287

• Vision, challenges and opportunities for a Plant Cell Atlas. eLife Plant Cell Atlas Consortium, Jha, S. G., Borowsky, A. T., Cole, B. J., Fahlgren, N., Farmer, A., Huang, S. C., Karia, P., Libault, M., Provart, N. J., Rice, S. L., Saura-Sanchez, M., Agarwal, P., Ahkami, A. H., Anderton, C. R., Briggs, S. P., Brophy, J. A., Denolf, P., Di Costanzo, L. F., Exposito-Alonso, M., Giacomello, S., Gomez-Cano, F., Kaufmann, K., Ko, D. K., Kumar, S., Malkovskiy, A. V., Nakayama, N., Obata, T., Otegui, M. S., Palfalvi, G., Quezada-Rodriguez, E. H., Singh, R., Uhrig, R. G., Waese, J., Van Wijk, K., Wright, R. C., Ehrhardt, D. W., Birnbaum, K. D., Rhee, S. Y., Ahmed, J., Alaba, O., Ameen, G., Arora, V., Arteaga-Vazquez, M. A., Arun, A., Bailey-Serres, J., Bartley, L. E., Bassel, G. W., Bergmann, D. C., Bertolini, E., Bhati, K. K., Blanco-Tourinan, N., Briggs, S. P., Brumos, J., Buer, B., Burlaocot, A., Cervantes-Perez, S. A., Chen, S., Contreras-Moreira, B., Corpas, F. J., Cruz-Ramirez, A., Cuevas-Velazquez, C. L., Cuperus, J. T., David, L. I., de Folter, S., Denolf, P. H., Ding, P., Dwyer, W. P., Evans, M. M., George, N., Handakumbura, P. P., Harrison, M. J., Haswell, E. S., Herath, V., Jiao, Y., Jinkerson, R. E., John, U., Joshi, S., Joshi, A., Joubert, L., Katam, R., Kaur, H., Kazachkova, Y., Raju, S. K., Khan, M. A., Khangura, R., Kumar, A., Kumar, A., Kumar, P., Kumar, P., Lavania, D., Lew, T. T., Lewsey, M. G., Lin, C., Liu, D., Liu, L., Liu, T., Lokdarshi, A., My Luong, A., Macaulay, I. C., Mahmud, S., Mahonen, A. P., Malukani, K. K., Marand, A. P., Martin, C. A., McWhite, C. D., Mehta, D., Martin, M. M., Mortimer, J. C., Nikolov, L. A., Nobori, T., Nolan, T. M., Ogden, A. J., Otegui, M. S., Ott, M., Palma, J. M., Paul, P., Rehman, A. U., Romera-Branchat, M., Romero, L. C., Roth, R., Sah, S. K., Shahan, R., Solanki, S., Song, B., Sozzani, R., Stacey, G., Stepanova, A. N., Taylor, N. L., Tello-Ruiz, M. K., Tran, T. M., Tripathi, R. K., Vadde, B. V., Varga, T., Vidovic, M., Walley, J. W., Wang, Z., Weizbauer, R. A., Whelan, J., Wijeratne, A. J., Xiang, T., Xu, S., Yadegari, R., Yu, H., Yuan, H. Y., Zanini, F., Zhao, F., Zhu, J., Zhuang, X. 2021; 10

  Abstract

  With growing populations and pressing environmental problems, future economies will be increasingly plant-based. Now is the time to reimagine plant science as a critical component of fundamental science, agriculture, environmental stewardship, energy, technology and healthcare. This effort requires a conceptual and technological framework to identify and map all cell types, and to comprehensively annotate the localization and organization of molecules at cellular and tissue levels. This framework, called the Plant Cell Atlas (PCA), will be critical for understanding and engineering plant development, physiology and environmental responses. A workshop was convened to discuss the purpose and utility of such an initiative, resulting in a roadmap that acknowledges the current knowledge gaps and technical challenges, and underscores how the PCA initiative can help to overcome them.

  View details for DOI 10.7554/eLife.66877

  View details for PubMedID 34491200

• Innovation, conservation, and repurposing of gene function in root cell type development CELL Kajala, K., Gouran, M., Shaar-Moshe, L., Mason, G., Rodriguez-Medina, J., Kawa, D., Pauluzzi, G., Reynoso, M., Canto-Pastor, A., Manzano, C., Lau, V., Artur, M. A. S., West, D. A., Gray, S. B., Borowsky, A. T., Moore, B. P., Yao, A., Morimoto, K. W., Bajic, M., Formentin, E., Nirmal, N. A., Rodriguez, A., Pasha, A., Deal, R. B., Kliebenstein, D. J., Hvidsten, T. R., Provart, N. J., Sinha, N. R., Runcie, D. E., Bailey-Serres, J., Brady, S. M. 2021; 184 (12): 3333-+

  Abstract

  Plant species have evolved myriads of solutions, including complex cell type development and regulation, to adapt to dynamic environments. To understand this cellular diversity, we profiled tomato root cell type translatomes. Using xylem differentiation in tomato, examples of functional innovation, repurposing, and conservation of transcription factors are described, relative to the model plant Arabidopsis. Repurposing and innovation of genes are further observed within an exodermis regulatory network and illustrate its function. Comparative translatome analyses of rice, tomato, and Arabidopsis cell populations suggest increased expression conservation of root meristems compared with other homologous populations. In addition, the functions of constitutively expressed genes are more conserved than those of cell type/tissue-enriched genes. These observations suggest that higher order properties of cell type and pan-cell type regulation are evolutionarily conserved between plants and animals.

  View details for DOI 10.1016/j.cell.2021.04.024

  View details for Web of Science ID 000660014300020

  View details for PubMedID 34010619

• Recurrent Loss of <i>abaA</i>, a Master Regulator of Asexual Development in Filamentous Fungi, Correlates with Changes in Genomic and Morphological Traits GENOME BIOLOGY AND EVOLUTION Mead, M. E., Borowsky, A. T., Joehnk, B., Steenwyk, J. L., Shen, X., Sil, A., Rokas, A. 2020; 12 (7): 1119-1130

  Abstract

  Gene regulatory networks (GRNs) drive developmental and cellular differentiation, and variation in their architectures gives rise to morphological diversity. Pioneering studies in Aspergillus fungi, coupled with subsequent work in other filamentous fungi, have shown that the GRN governed by the BrlA, AbaA, and WetA proteins controls the development of the asexual fruiting body or conidiophore. A specific aspect of conidiophore development is the production of phialides, conidiophore structures that are under the developmental control of AbaA and function to repetitively generate spores. Fungal genome sequencing has revealed that some filamentous fungi lack abaA, and also produce asexual structures that lack phialides, raising the hypothesis that abaA loss is functionally linked to diversity in asexual fruiting body morphology. To examine this hypothesis, we carried out an extensive search for the abaA gene across 241 genomes of species from the fungal subphylum Pezizomycotina. We found that abaA was independently lost in four lineages of Eurotiomycetes, including from all sequenced species within the order Onygenales, and that all four lineages that have lost abaA also lack the ability to form phialides. Genetic restoration of abaA from Aspergillus nidulans into Histoplasma capsulatum, a pathogenic species from the order Onygenales that lacks an endogenous copy of abaA, did not alter Histoplasma conidiation morphology but resulted in a marked increase in spore viability. We also discovered that species lacking abaA contain fewer AbaA binding motifs in the regulatory regions of orthologs of some AbaA target genes, suggesting that the asexual fruiting body GRN of organisms that have lost abaA has likely been rewired. Our results provide an illustration of how repeated losses of a key regulatory transcription factor have contributed to the diversity of an iconic fungal morphological trait.

  View details for DOI 10.1093/gbe/evaa107

  View details for Web of Science ID 000582693800014

  View details for PubMedID 32442273

  View details for PubMedCentralID PMC7531577

• A Global Coexpression Network Approach for Connecting Genes to Specialized Metabolic Pathways in Plants PLANT CELL Wisecaver, J. H., Borowsky, A. T., Tzin, V., Jander, G., Kliebenstein, D. J., Rokas, A. 2017; 29 (5): 944-959

  Abstract

  Plants produce diverse specialized metabolites (SMs), but the genes responsible for their production and regulation remain largely unknown, hindering efforts to tap plant pharmacopeia. Given that genes comprising SM pathways exhibit environmentally dependent coregulation, we hypothesized that genes within a SM pathway would form tight associations (modules) with each other in coexpression networks, facilitating their identification. To evaluate this hypothesis, we used 10 global coexpression data sets, each a meta-analysis of hundreds to thousands of experiments, across eight plant species to identify hundreds of coexpressed gene modules per data set. In support of our hypothesis, 15.3 to 52.6% of modules contained two or more known SM biosynthetic genes, and module genes were enriched in SM functions. Moreover, modules recovered many experimentally validated SM pathways, including all six known to form biosynthetic gene clusters (BGCs). In contrast, bioinformatically predicted BGCs (i.e., those lacking an associated metabolite) were no more coexpressed than the null distribution for neighboring genes. These results suggest that most predicted plant BGCs are not genuine SM pathways and argue that BGCs are not a hallmark of plant specialized metabolism. We submit that global gene coexpression is a rich, largely untapped resource for discovering the genetic basis and architecture of plant natural products.

  View details for DOI 10.1105/tpc.17.00009

  View details for Web of Science ID 000402860900005

  View details for PubMedID 28408660

  View details for PubMedCentralID PMC5466033