Science Forum: Vision, challenges and opportunities for a Plant Cell Atlas

  1. Plant Cell Atlas Consortium
  2. Suryatapa Ghosh Jha
  3. Alexander T Borowsky
  4. Benjamin J Cole
  5. Noah Fahlgren
  6. Andrew Farmer
  7. Shao-shan Carol Huang
  8. Purva Karia
  9. Marc Libault
  10. Nicholas J Provart
  11. Selena L Rice
  12. Maite Saura-Sanchez
  13. Pinky Agarwal
  14. Amir H Ahkami
  15. Christopher R Anderton
  16. Steven P Briggs
  17. Jennifer AN Brophy
  18. Peter Denolf
  19. Luigi F Di Costanzo
  20. Moises Exposito-Alonso
  21. Stefania Giacomello
  22. Fabio Gomez-Cano
  23. Kerstin Kaufmann
  24. Dae Kwan Ko
  25. Sagar Kumar
  26. Andrey V Malkovskiy
  27. Naomi Nakayama
  28. Toshihiro Obata
  29. Marisa S Otegui
  30. Gergo Palfalvi
  31. Elsa H Quezada-Rodríguez
  32. Rajveer Singh
  33. R Glen Uhrig
  34. Jamie Waese
  35. Klaas Van Wijk
  36. R Clay Wright
  37. David W Ehrhardt  Is a corresponding author
  38. Kenneth D Birnbaum  Is a corresponding author
  39. Seung Y Rhee  Is a corresponding author
  1. Plant Cell Atlas, United States
  2. Department of Plant Biology, Carnegie Institution for Science, United States
  3. Department of Botany and Plant Sciences, University of California, Riverside, United States
  4. Joint Genome Institute, Lawrence Berkeley National Laboratory, United States
  5. Donald Danforth Plant Science Center, United States
  6. National Center for Genome Resources, United States
  7. Center for Genomics and Systems Biology, New York University, United States
  8. Department of Cell and Systems Biology, University of Toronto, Canada
  9. Department of Agronomy and Horticulture, University of Nebraska-Lincoln, United States
  10. Department of Cell and Systems Biology and the Centre for the Analysis of Genome Evolution and Function, University of Toronto, Canada
  11. Consejo Nacional de Investigaciones Científicas y Técnicas, Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura, Facultad de Agronomía, Universidad de Buenos Aires, Argentina
  12. National Institute of Plant Genome Research, India
  13. Environmental Molecular Sciences Division, Pacific Northwest National Laboratory, United States
  14. Department of Biological Sciences, University of California, San Diego, United States
  15. Department of Biology, Stanford University, United States
  16. BASF Seeds & Traits, Belgium
  17. Department of Agricultural Sciences, University of Naples Federico II, Italy
  18. Department of Plant Biology, Carnegie Institution for Science, Germany
  19. SciLifeLab, KTH Royal Institute of Technology, Sweden
  20. Department of Biochemistry and Molecular Biology, Michigan State University, United States
  21. Department for Plant Cell and Molecular Biology, Institute for Biology, Humboldt-Universitaet zu Berlin, Germany
  22. Great Lakes Bioenergy Research Center, Michigan State University, United States
  23. Department of Plant Breeding & Genetics, Mata Gujri College, Fatehgarh Sahib, Punjabi University, India
  24. Department of Bioengineering, Imperial College London, United Kingdom
  25. Department of Biochemistry, University of Nebraska-Lincoln, United States
  26. Department of Botany, University of Wisconsin-Madison, United States
  27. Division of Evolutionary Biology, National Institute for Basic Biology, Japan
  28. Ciencias Agrogenómicas, Escuela Nacional de Estudios Superiores Unidad León, Universidad Nacional Autónoma de México, Mexico
  29. School of Agricultural Biotechnology, Punjab Agricultural University, India
  30. Department of Science, University of Alberta, Canada
  31. Department of Cell and Systems Biology/Centre for the Analysis of Genome Evolution and Function, University of Toronto, Canada
  32. School of Integrated Plant Science, Plant Biology Section, Cornell University, United States
  33. Department of Biological Systems Engineering, Virginia Tech, United States
7 figures

Figures

Location-to-function paradigm.

The illustration shows the levels of organization of a plant (left) and a few examples highlight how location determines function at each level (right). At the molecular level, functions of protein complexes can be determined by their localization in membrane microdomains (Jarsch et al., 2014) or by dynamic protein interactions (Obata, 2019). At the cellular level, a protein can be located differentially through transport mechanisms, including vesicle trafficking (Goring and Di Sansebastiano, 2018) and nuclear translocation (Marchive et al., 2013), regulating its function. At the tissue level, cell position can drive its fate into a specialized cell type (Shao and Dong, 2016). Metabolic pathways can operate specifically in specialized cell types across tissues (Marchive et al., 2013; Schlüter and Weber, 2020). At the next level, the existence of non-cell-autonomous transcription factors can transverse intercellular scales across plant organs (Han et al., 2014). Also, an organ-dependent post-translational proteome has been described as a mechanism of protein function regulation (Uhrig et al., 2019). At the organism level, plant interaction with biotic (Harrison et al., 2002) and abiotic factors (Michaud et al., 2017) can occur through a localized cue perception.

PCA milestones.

PCA milestones for the next 10 years and beyond in data generation (yellow bars), data analysis (purple bars), software development (green bars), and building PCA community (orange bar).

A conceptual diagram of a PCA user interface.

An example of a PCA user interface that integrates various data types from molecular, biochemical, cellular and evolutionary contexts to connect location to function. Shown are example data types that would be seamlessly connected to enable easy navigation and discovery (FL: fluorescence).

People and culture.

Major stakeholders of the PCA are described. The goal is to establish a broad network of collaboration between developers and users through the creation of an accessible platform, educational tools and outreach activities. The PCA community should strive to be inclusive, diverse and transparent.

PCA research framework.

Building the PCA will require cooperation and coordination between plant science, technology and data infrastructure. Plant scientists will use new technologies to generate data at the single-cell level, which will be integrated by data scientists into the PCA infrastructure through manual and automated curation. This data integration will enable the development of new technologies and drive new hypotheses and investigations for plant scientists, who will then contribute additional data to the PCA resource.

Knowledge gaps to fill for the PCA.

Several limitations inherent to plants (shown as pieces of a jigsaw puzzle) must be overcome to enhance the understanding of plant cells as biological systems. To characterize the unique molecular attributes of each cell type composing a plant, plant biologists will need to develop reliable methods to broadly access the different cell types across various plant species. Also, single-cell multi-omics technologies will be necessary to get a deeper understanding of plant cell processes across all layers of molecular regulation. This data must be gained in the context of functional annotation of the cells. This would require the identification of reliable marker genes for each type of plant cell-. Ultimately, the spatiotemporal distribution of the molecular attributes of each cell will help to understand their dynamic regulation during plant cell development and in response to environmental stresses. Integrating the information collected using bioinformatics tools will enable the characterization of regulatory networks at a single-cell resolution and comparative analyses across plant species at the cellular level. This data will fuel the establishment of new synthetic biology strategies to enhance plant biology.

The chloroplast structure and function in connection to location.

The PCA could facilitate an increased understanding of the biology of the chloroplast by providing accessible, integrative and spatially-resolved data for transcripts, proteins and metabolites across cell types (Box 2). (A) A representation of a typical chloroplast structure and its compartments. (B) The chloroplast structural differences in some plant lineage. (C) A leaf cross-section showing different chloroplast location at the tissue level in land and aquatic plants. (D) The chloroplast location can change within the cell upon environmental cues such as light intensity. (E) Various forms of chloroplasts in different organs.

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  1. Plant Cell Atlas Consortium
  2. Suryatapa Ghosh Jha
  3. Alexander T Borowsky
  4. Benjamin J Cole
  5. Noah Fahlgren
  6. Andrew Farmer
  7. Shao-shan Carol Huang
  8. Purva Karia
  9. Marc Libault
  10. Nicholas J Provart
  11. Selena L Rice
  12. Maite Saura-Sanchez
  13. Pinky Agarwal
  14. Amir H Ahkami
  15. Christopher R Anderton
  16. Steven P Briggs
  17. Jennifer AN Brophy
  18. Peter Denolf
  19. Luigi F Di Costanzo
  20. Moises Exposito-Alonso
  21. Stefania Giacomello
  22. Fabio Gomez-Cano
  23. Kerstin Kaufmann
  24. Dae Kwan Ko
  25. Sagar Kumar
  26. Andrey V Malkovskiy
  27. Naomi Nakayama
  28. Toshihiro Obata
  29. Marisa S Otegui
  30. Gergo Palfalvi
  31. Elsa H Quezada-Rodríguez
  32. Rajveer Singh
  33. R Glen Uhrig
  34. Jamie Waese
  35. Klaas Van Wijk
  36. R Clay Wright
  37. David W Ehrhardt
  38. Kenneth D Birnbaum
  39. Seung Y Rhee
(2021)
Science Forum: Vision, challenges and opportunities for a Plant Cell Atlas
eLife 10:e66877.
https://doi.org/10.7554/eLife.66877