Single-Cell Omics in Crop Plants: Opportunities and Challenges

Abstract Omics studies in plants have helped in the molecular characterization of whole plants or their organs. However, these studies lack information on cellular behavior, cell-to-cell variations, and distinct molecular program(s) operational in individual cells. As an enormous variability exists owing to the type and developmental stage of plant cell/tissue(s), the multidimensionality and complexity of cellular responses in plants towards the environment and growth stages requires descaling to single-cell-type omics technologies to dissect the complex responses to obtain concrete information of components at the ultrastructural, subcellular, or organellar hierarchies of the genome, transcriptome, proteome, and metabolome pathways. Further, single-cell multiomics studies aiming at simultaneous extraction and analysis of different analyte biomolecules in a cell will help in validating the relative changes occurring in a cell to a specific event or elicitor. The integration of the four different omics data and development of an interactome having nodes and edges will then help in designing a comprehensive regulatory system operating in an individual cell. The near complete integrative information on the working and operations of emphatic plant biological systems will furnish us with the ingenuity to design climate-ready resilient crops to cope with the aberrant environmental stresses.

[1]  Aleksandra A. Kolodziejczyk,et al.  The technology and biology of single-cell RNA sequencing. , 2015, Molecular cell.

[2]  A. Melchinger,et al.  Beyond Genomic Prediction: Combining Different Types of omics Data Can Improve Prediction of Hybrid Performance in Maize , 2018, Genetics.

[3]  Sichun Zhang,et al.  Single cell analysis with probe ESI-mass spectrometry: detection of metabolites at cellular and subcellular levels. , 2014, Analytical chemistry.

[4]  Zhangjun Fei,et al.  High-resolution spatiotemporal transcriptome mapping of tomato fruit development and ripening , 2018, Nature Communications.

[5]  Sixue Chen,et al.  Metabolomics and Proteomics of Brassica napus Guard Cells in Response to Low CO2 , 2017, Front. Mol. Biosci..

[6]  Sixue Chen,et al.  Single-cell-type Proteomics: Toward a Holistic Understanding of Plant Function* , 2012, Molecular & Cellular Proteomics.

[7]  M. Kubista,et al.  Platforms for Single-Cell Collection and Analysis , 2018, International journal of molecular sciences.

[8]  R. Satija,et al.  Root Regeneration Triggers an Embryo-like Sequence Guided by Hormonal Interactions , 2016, Cell.

[9]  Scott I. Hsieh,et al.  Systems Biology Approach in Chlamydomonas Reveals Connections between Copper Nutrition and Multiple Metabolic Steps[C][W][OA] , 2011, Plant Cell.

[10]  Jan Vrána,et al.  Advances in plant chromosome genomics. , 2014, Biotechnology advances.

[11]  K. Hodne,et al.  Single-Cell Isolation and Gene Analysis: Pitfalls and Possibilities , 2015, International journal of molecular sciences.

[12]  J. Schiefelbein Molecular phenotyping of plant single cell-types enhances forward genetic analyses , 2015, Front. Plant Sci..

[13]  U. Grossniklaus,et al.  The female gametophyte: an emerging model for cell type-specific systems biology in plant development , 2015, Front. Plant Sci..

[14]  Lia Chappell,et al.  Single-Cell (Multi)omics Technologies. , 2018, Annual review of genomics and human genetics.

[15]  Aleksandra A. Kolodziejczyk,et al.  Global and targeted approaches to single-cell transcriptome characterization , 2017, Briefings in functional genomics.

[16]  Suping Zhou,et al.  Development of a laser capture microscope-based single-cell-type proteomics tool for studying proteomes of individual cell layers of plant roots , 2016, Horticulture Research.

[17]  T. Masujima,et al.  Live Single-Cell Plant Hormone Analysis by Video-Mass Spectrometry. , 2015, Plant & cell physiology.

[18]  Tai Wang,et al.  Methods to isolate a large amount of generative cells, sperm cells and vegetative nuclei from tomato pollen for “omics” analysis , 2015, Front. Plant Sci..

[19]  D. Cozzolino,et al.  Handling Complexity in Animal and Plant Science Research—From Single to Functional Traits: Are We There Yet? , 2018, High-throughput.

[20]  J. Rose,et al.  Laser microdissection of tomato fruit cell and tissue types for transcriptome profiling , 2016, Nature Protocols.

[21]  P. Ahmad,et al.  Role of Proteomics in Crop Stress Tolerance , 2016, Front. Plant Sci..

[22]  J. Schiefelbein,et al.  Plant Systems Biology at the Single-Cell Level. , 2017, Trends in plant science.

[23]  Biswapriya B Misra,et al.  Plant single-cell and single-cell-type metabolomics. , 2014, Trends in plant science.

[24]  M. Libault,et al.  Decipher the Molecular Response of Plant Single Cell Types to Environmental Stresses , 2016, BioMed research international.

[25]  Xiaoling Wu,et al.  Enhancing Omics Research of Crop Responses to Drought under Field Conditions , 2017, Front. Plant Sci..

[26]  R. Vera-Estrella,et al.  Single-cell-type quantitative proteomic and ionomic analysis of epidermal bladder cells from the halophyte model plant Mesembryanthemum crystallinum to identify salt-responsive proteins , 2016, BMC Plant Biology.

[27]  Jie Luo,et al.  Rewiring of the Fruit Metabolome in Tomato Breeding , 2018, Cell.

[28]  Bing-Yun Yu,et al.  OMICS Technologies and Applications in Sugar Beet , 2016, Front. Plant Sci..

[29]  J. Emon The Omics Revolution in Agricultural Research. , 2016 .

[30]  K. Birnbaum,et al.  Quantification of cell identity from single-cell gene expression profiles , 2015, Genome Biology.

[31]  Maojun Wang,et al.  Multi-omics maps of cotton fibre reveal epigenetic basis for staged single-cell differentiation , 2016, Nucleic acids research.

[32]  W. Gruissem,et al.  Proteasome targeting of proteins in Arabidopsis leaf mesophyll, epidermal and vascular tissues , 2015, Front. Plant Sci..

[33]  M. Taoka,et al.  Identification of Proteins Enriched in Rice Egg or Sperm Cells by Single-Cell Proteomics , 2013, PloS one.

[34]  David A. Weitz,et al.  Scaling by shrinking: empowering single-cell 'omics' with microfluidic devices , 2017, Nature Reviews Genetics.

[35]  Shaohua Li,et al.  Integrating Omics and Alternative Splicing Reveals Insights into Grape Response to High Temperature1[OPEN] , 2017, Plant Physiology.

[36]  Dominik K. Grosskinsky,et al.  Integration of multi-omics techniques and physiological phenotyping within a holistic phenomics approach to study senescence in model and crop plants. , 2018, Journal of experimental botany.

[37]  W. Schulze,et al.  Early nitrogen-deprivation responses in Arabidopsis roots reveal distinct differences on transcriptome and (phospho-) proteome levels between nitrate and ammonium nutrition. , 2016, The Plant journal : for cell and molecular biology.

[38]  Sagar M. Utturkar,et al.  Enrichment of Root Endophytic Bacteria from Populus deltoides and Single-Cell-Genomics Analysis , 2016, Applied and Environmental Microbiology.

[39]  S. Linnarsson,et al.  Single-cell genomics: coming of age , 2016, Genome Biology.

[40]  Andrew Liu,et al.  Application of multi-omics in single cells , 2018 .

[41]  D. Edwards,et al.  Single-Cell Genomic Analysis in Plants , 2018, Genes.

[42]  Kenneth D. Birnbaum,et al.  The potential of single-cell profiling in plants , 2016, Genome Biology.