Vision, challenges and opportunities for a Plant Cell Atlas.

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

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.

Keywords

References

  1. Plant Physiol. 2010 Feb;152(2):500-15 [PMID: 20007449]
  2. Nat Commun. 2021 Oct 7;12(1):5890 [PMID: 34620862]
  3. Nucleic Acids Res. 2019 Jan 8;47(D1):D520-D528 [PMID: 30357364]
  4. Plant Direct. 2020 Sep 01;4(8):e00252 [PMID: 32904806]
  5. Plant Cell. 2017 Aug;29(8):1806-1821 [PMID: 28808136]
  6. Nat Genet. 2012 Jan 27;44(2):121-6 [PMID: 22281772]
  7. Plant Cell. 2019 Jul;31(7):1614-1632 [PMID: 31123051]
  8. Elife. 2017 Dec 05;6: [PMID: 29206104]
  9. Philos Trans R Soc Lond B Biol Sci. 2018 Sep 10;373(1758): [PMID: 30201845]
  10. FEBS Lett. 2018 Nov;592(22):3653-3657 [PMID: 30426476]
  11. Nature. 2021 Apr;592(7852):110-115 [PMID: 33692545]
  12. Plant J. 2019 Jul;99(1):176-194 [PMID: 30920011]
  13. Nat Commun. 2020 Sep 25;11(1):4879 [PMID: 32978379]
  14. Nature. 2020 Nov;587(7832):152-156 [PMID: 33087931]
  15. Proc Natl Acad Sci U S A. 2018 Apr 10;115(15):3804-3809 [PMID: 29581251]
  16. PLoS One. 2015 Sep 15;10(9):e0138176 [PMID: 26372555]
  17. Plant Physiol. 2007 Feb;143(2):587-99 [PMID: 17142475]
  18. Development. 2019 Jun 27;146(12): [PMID: 31249003]
  19. Ann Bot. 2020 May 13;125(6):869-879 [PMID: 31942934]
  20. Methods Mol Biol. 2018;1829:73-85 [PMID: 29987715]
  21. Cell. 2021 Jun 10;184(12):3333-3348.e19 [PMID: 34010619]
  22. Trends Biotechnol. 2020 Sep;38(9):1007-1022 [PMID: 32818441]
  23. Elife. 2019 Sep 19;8: [PMID: 31535972]
  24. Front Comput Neurosci. 2014 Nov 03;8:137 [PMID: 25404913]
  25. Proc Natl Acad Sci U S A. 2018 Nov 6;115(45):E10778-E10787 [PMID: 30352850]
  26. Plant Physiol. 2020 Feb;182(2):692-706 [PMID: 31818904]
  27. J Exp Bot. 2014 Apr;65(7):1737-49 [PMID: 24347464]
  28. Nucleic Acids Res. 2005 Jan 1;33(Database issue):D562-6 [PMID: 15608262]
  29. Plant Biotechnol J. 2016 May;14(5):1241-50 [PMID: 26503031]
  30. Cell. 2018 Aug 9;174(4):1015-1030.e16 [PMID: 30096299]
  31. Plant Signal Behav. 2008 Jun;3(6):367-75 [PMID: 19513224]
  32. Annu Rev Plant Biol. 2004;55:173-96 [PMID: 15377218]
  33. Curr Opin Biotechnol. 2019 Oct;59:8-15 [PMID: 30798145]
  34. Nucleic Acids Res. 2020 Jan 8;48(D1):D1063-D1068 [PMID: 31642487]
  35. Nucleic Acids Res. 2017 Jan 4;45(D1):D1100-D1106 [PMID: 27924013]
  36. Cell. 2018 Aug 9;174(4):999-1014.e22 [PMID: 30096314]
  37. J Exp Bot. 2017 Dec 18;69(1):1-5 [PMID: 29267941]
  38. Nat Commun. 2020 Jun 29;11(1):3284 [PMID: 32601292]
  39. Mol Plant. 2019 May 6;12(5):648-660 [PMID: 31004836]
  40. Plant Direct. 2020 Oct 15;4(10):e00271 [PMID: 33083684]
  41. Cell. 2019 Dec 12;179(7):1455-1467 [PMID: 31835027]
  42. Plant Cell Rep. 2020 Jan;39(1):163-167 [PMID: 31754780]
  43. Nucleic Acids Res. 2010 Jan;38(Database issue):D33-8 [PMID: 19850725]
  44. Nat Methods. 2022 Feb;19(2):171-178 [PMID: 35102346]
  45. Nat Genet. 2008 Nov;40(11):1370-4 [PMID: 18820698]
  46. Science. 2018 Apr 13;360(6385):176-182 [PMID: 29545511]
  47. New Phytol. 2020 Jul;227(1):260-273 [PMID: 32171029]
  48. Genome Biol. 2005;6(2):R21 [PMID: 15693950]
  49. Curr Protoc. 2021 May;1(5):e153 [PMID: 34043287]
  50. Glob Chang Biol. 2020 Jan;26(1):274-286 [PMID: 31642554]
  51. Nucleic Acids Res. 2017 Jan 4;45(D1):D1054-D1059 [PMID: 27924043]
  52. Plant J. 2019 Nov;100(3):641-654 [PMID: 31350781]
  53. Plant Cell. 2019 Dec;31(12):2868-2887 [PMID: 31562216]
  54. Elife. 2020 Mar 24;9: [PMID: 32208137]
  55. Nat Chem Biol. 2019 Nov;15(11):1110-1119 [PMID: 31591565]
  56. Science. 2018 Apr 13;360(6385):212-215 [PMID: 29519919]
  57. Nat Plants. 2017 May 08;3:17061 [PMID: 28481330]
  58. New Phytol. 2021 May;230(3):931-937 [PMID: 33452833]
  59. Sci Data. 2016 Mar 15;3:160018 [PMID: 26978244]
  60. Plant J. 2021 Jan;105(2):542-557 [PMID: 33231903]
  61. Nat Methods. 2019 Dec;16(12):1289-1296 [PMID: 31740819]
  62. Nucleic Acids Res. 2018 Jan 4;46(D1):D1150-D1156 [PMID: 29059333]
  63. Nat Protoc. 2007;2(7):1565-72 [PMID: 17585298]
  64. Nat Commun. 2013;4:1713 [PMID: 23591880]
  65. Methods Mol Biol. 2018;1829:55-72 [PMID: 29987714]
  66. Plant Cell Rep. 2019 Jul;38(7):819-823 [PMID: 30671650]
  67. Nature. 2013 Mar 21;495(7441):305-7 [PMID: 23518546]
  68. Nat Commun. 2019 Jul 19;10(1):3252 [PMID: 31324801]
  69. Nature. 2020 May;581(7807):221-224 [PMID: 32225175]
  70. Nat Biotechnol. 2019 Jun;37(6):685-691 [PMID: 31061482]
  71. Annu Rev Plant Biol. 2020 Apr 29;71:183-215 [PMID: 32131603]
  72. Plant Cell. 2015 Aug;27(8):2119-32 [PMID: 26265761]
  73. Plant Physiol. 2019 Mar;179(3):794-802 [PMID: 30181342]
  74. Proc Natl Acad Sci U S A. 2017 Jul 11;114(28):7444-7449 [PMID: 28652343]
  75. Nat Commun. 2020 Jul 10;11(1):3439 [PMID: 32651385]
  76. Plant Cell. 2019 Dec;31(12):3015-3032 [PMID: 31597687]
  77. Nucleic Acids Res. 2019 Jan 8;47(D1):D1146-D1154 [PMID: 30407532]
  78. Cell Mol Life Sci. 2020 Jan;77(2):275-287 [PMID: 31422442]
  79. Curr Opin Plant Biol. 2021 Apr;60:102041 [PMID: 33915520]
  80. Proc Natl Acad Sci U S A. 2018 May 8;115(19):4887-4890 [PMID: 29686094]
  81. J Biomed Semantics. 2016 Jul 04;7(1):44 [PMID: 27377652]
  82. Int J Biol Macromol. 2018 May;111:400-414 [PMID: 29305884]
  83. Nat Commun. 2020 Sep 25;11(1):4880 [PMID: 32978375]
  84. Plant Biotechnol J. 2016 Nov;14(11):2079-2099 [PMID: 27442628]
  85. Nat Plants. 2020 Jul;6(7):766-772 [PMID: 32601420]
  86. Trends Plant Sci. 2010 Nov;15(11):641-50 [PMID: 20851035]
  87. J Exp Bot. 2017 Jun 1;68(14):3773-3784 [PMID: 28911056]
  88. Dev Biol. 2016 Nov 1;419(1):121-131 [PMID: 27475487]
  89. Curr Opin Plant Biol. 2020 Apr;54:114-121 [PMID: 32388018]
  90. Genesis. 2015 Aug;53(8):474-85 [PMID: 26201819]
  91. Proc Natl Acad Sci U S A. 2020 Sep 1;117(35):21796-21803 [PMID: 32817419]
  92. Nat Biotechnol. 2016 Aug 9;34(8):828-837 [PMID: 27504778]
  93. Plant Cell. 2014 Apr 8;26(4):1698-1711 [PMID: 24714763]
  94. Proc Natl Acad Sci U S A. 2020 Oct 13;117(41):25880-25889 [PMID: 32989160]
  95. Plant Cell. 2002 Oct;14(10):2413-29 [PMID: 12368495]
  96. Mol Plant. 2021 Mar 1;14(3):372-383 [PMID: 33422696]
  97. Nucleic Acids Res. 2008 Jan;36(Database issue):D449-54 [PMID: 18194960]
  98. Genome Biol. 2001;2(8):REPORTS4019 [PMID: 11532210]
  99. Redox Biol. 2020 Oct;37:101717 [PMID: 32979794]
  100. Trends Biochem Sci. 2020 Feb;45(2):123-136 [PMID: 31753702]
  101. Nucleic Acids Res. 2020 Jan 8;48(D1):D689-D695 [PMID: 31598706]
  102. Science. 2019 Sep 27;365(6460):1461-1466 [PMID: 31604275]
  103. Science. 2019 Sep 27;365(6460):1401-1405 [PMID: 31604266]
  104. Curr Opin Plant Biol. 2017 Oct;39:129-135 [PMID: 28750256]
  105. Cell. 2018 Feb 22;172(5):1091-1107.e17 [PMID: 29474909]
  106. Curr Opin Plant Biol. 2016 Jun;31:76-82 [PMID: 27061048]
  107. Biochim Biophys Acta. 2014 Apr;1837(4):522-30 [PMID: 24333784]
  108. Cell. 2019 Jun 13;177(7):1888-1902.e21 [PMID: 31178118]
  109. New Phytol. 2019 Feb;221(3):1197-1214 [PMID: 30222198]
  110. Nucleic Acids Res. 2012 Jan;40(Database issue):D1178-86 [PMID: 22110026]
  111. Int J Mass Spectrom. 2020 Dec;458: [PMID: 33162786]
  112. F1000Res. 2019 Oct 18;8:1775 [PMID: 32399185]
  113. Nature. 2006 Nov 16;444(7117):323-9 [PMID: 17108957]
  114. Trends Plant Sci. 2017 Nov;22(11):949-960 [PMID: 28970001]
  115. N Biotechnol. 2019 Jul 25;51:49-56 [PMID: 30779963]
  116. Nucleic Acids Res. 2011 Jan;39(Database issue):D28-31 [PMID: 20972220]
  117. PLoS Biol. 2011 Apr;9(4):e1001046 [PMID: 21526222]
  118. Trends Plant Sci. 2019 Oct;24(10):917-926 [PMID: 31300194]
  119. Nature. 2018 Oct;562(7727):367-372 [PMID: 30283141]
  120. Nucleic Acids Res. 2019 Jan 8;47(D1):D330-D338 [PMID: 30395331]
  121. Front Plant Sci. 2020 Jan 10;10:1629 [PMID: 31998331]
  122. Biochim Biophys Acta Mol Cell Res. 2021 Apr;1868(5):118949 [PMID: 33421532]
  123. Genome Biol. 2020 Feb 7;21(1):31 [PMID: 32033589]
  124. Mycorrhiza. 2006 Jul;16(5):299-363 [PMID: 16845554]
  125. Development. 2015 Feb 1;142(3):420-30 [PMID: 25605778]
  126. Nucleic Acids Res. 2020 Jan 8;48(D1):D77-D83 [PMID: 31665515]
  127. Nat Biotechnol. 2023 Sep 7;: [PMID: 37679542]
  128. Nucleic Acids Res. 2007 Jan;35(Database issue):D863-9 [PMID: 17130150]
  129. Plant Physiol. 2020 Mar;182(3):1194-1210 [PMID: 31911558]
  130. Curr Opin Plant Biol. 2018 Apr;42:30-36 [PMID: 29459221]
  131. Science. 2007 Feb 9;315(5813):804-7 [PMID: 17289988]
  132. Nucleic Acids Res. 2021 Jan 8;49(D1):D1452-D1463 [PMID: 33170273]
  133. Plant Physiol. 2020 Oct;184(2):1056-1071 [PMID: 32769161]
  134. Brief Bioinform. 2021 May 20;22(3): [PMID: 34020545]
  135. Nat Commun. 2021 Mar 26;12(1):1901 [PMID: 33772008]
  136. PLoS Comput Biol. 2018 Jan 29;14(1):e1005968 [PMID: 29377902]
  137. Nat Commun. 2021 May 20;12(1):2739 [PMID: 34016974]
  138. Cell. 2021 May 27;184(11):3041-3055.e21 [PMID: 33964211]
  139. Structure. 2017 Aug 1;25(8):1222-1232.e3 [PMID: 28669634]
  140. Trends Plant Sci. 2017 Dec;22(12):1001-1003 [PMID: 29029828]
  141. Nucleic Acids Res. 2018 Jan 4;46(D1):D8-D13 [PMID: 29140470]

Grants

  1. R01 GM123259/NIGMS NIH HHS
  2. R35 GM138143/NIGMS NIH HHS

MeSH Term

Agriculture
Chlamydomonas reinhardtii
Chloroplasts
Computational Biology
Image Processing, Computer-Assisted
Plant Cells
Plant Development
Plants
Zea mays

Word Cloud

Created with Highcharts 10.0.0environmentalsciencePlantCellAtlaswillplantcriticalframeworkcellPCAinitiativechallengesgrowingpopulationspressingproblemsfutureeconomiesincreasinglyplant-basedNowtimereimaginecomponentfundamentalagriculturestewardshipenergytechnologyhealthcareeffortrequiresconceptualtechnologicalidentifymaptypescomprehensivelyannotatelocalizationorganizationmoleculescellulartissuelevelscalledunderstandingengineeringdevelopmentphysiologyresponsesworkshopconveneddiscusspurposeutilityresultingroadmapacknowledgescurrentknowledgegapstechnicalunderscorescanhelpovercomethemVisionopportunities4Dimagingthalianabiologychlamydomonasreinhardtiilocation-to-functionmaizeforumsingle-cellomicstranslationalresearch

Similar Articles

Cited By (23)