Abstract
In multicellular and even single-celled organisms, individual components are interconnected at multiscale levels to produce enormously complex biological networks that help these systems maintain homeostasis for development and environmental adaptation. Systems biology studies initially adopted network analysis to explore how relationships between individual components give rise to complex biological processes. Network analysis has been applied to dissect the complex connectivity of mammalian brains across different scales in time and space in The Human Brain Project. In plant science, network analysis has similarly been applied to study the connectivity of plant components at the molecular, subcellular, cellular, organic, and organism levels. Analysis of these multiscale networks contributes to our understanding of how genotype determines phenotype. In this review, we summarized the theoretical framework of plant multiscale networks and introduced studies investigating plant networks by various experimental and computational modalities. We next discussed the currently available analytic methodologies and multi-level imaging techniques used to map multiscale networks in plants. Finally, we highlighted some of the technical challenges and key questions remaining to be addressed in this emerging field.
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Abrahamsson, S., Chen, J., Hajj, B., Stallinga, S., Katsov, A.Y., Wisniewski, J., Mizuguchi, G., Soule, P., Mueller, F., Dugast Darzacq, C., et al. (2013). Fast multicolor 3D imaging using aberration-corrected multifocus microscopy. Nat Methods 10, 60–63.
Alejandro, S., Lee, Y., Tohge, T., Sudre, D., Osorio, S., Park, J., Bovet, L., Lee, Y., Geldner, N., Fernie, A.R., et al. (2012). AtABCG29 is a monolignol transporter involved in lignin biosynthesis. Curr Biol 22, 1207–1212.
Ali, O., Mirabet, V., Godin, C., and Traas, J. (2014). Physical models of plant development. Annu Rev Cell Dev Biol 30, 59–78.
Allen, W.E. (2020). Brain mapping, from molecules to networks. Science 370, 925.3–925.
Altmann, M., Altmann, S., Rodriguez, P.A., Weller, B., Elorduy Vergara, L., Palme, J., Marín-de la Rosa, N., Sauer, M., Wenig, M., Villaécija-Aguilar, J.A., et al. (2020). Extensive signal integration by the phytohormone protein network. Nature 583, 271–276.
Amunts, K., Mohlberg, H., Bludau, S., and Zilles, K. (2020). Julich-Brain: A 3D probabilistic atlas of the human brain’s cytoarchitecture. Science 369, 988–992.
Arabidopsis Genome Initiative, (2000). Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796–815.
Bacete, L., and Hamann, T. (2020). The role of mechanoperception in plant cell wall integrity maintenance. Plants 9, 574.
Bang, B.G., and Bang, F.B. (1957). Graphic reconstruction of the third dimension from serial electron microphotographs. J Ultrastruct Res 1, 138–146.
Barbier de Reuille, P., Routier-Kierzkowska, A.L., Kierzkowski, D., Bassel, G.W., Schüpbach, T., Tauriello, G., Bajpai, N., Strauss, S., Weber, A., Kiss, A., et al. (2015). MorphoGraphX: A platform for quantifying morphogenesis in 4D. eLife 4, e05864.
Bassel, G.W. (2018). Information processing and distributed computation in plant organs. Trends Plant Sci 23, 994–1005.
Bassel, G.W. (2019). Multicellular systems biology: quantifying cellular patterning and function in plant organs using network science. Mol Plant 12, 731–742.
Bassel, G.W., Stamm, P., Mosca, G., Barbier de Reuille, P., Gibbs, D.J., Winter, R., Janka, A., Holdsworth, M.J., and Smith, R.S. (2014). Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo. Proc Natl Acad Sci USA 111, 8685–8690.
Ben-Tabou de-Leon, S., and Davidson, E.H. (2007). Gene regulation: gene control network in development. Annu Rev Biophys Biomol Struct 36, 191–212.
Benfey, P.N. (2012). Toward a systems analysis of the root. Cold Spring Harb Symp Quant Biol 77, 91–96.
Birch-Andersen, A. (1955). Reconstruction of the nuclear sites of Salmonella typhimurium from electron micrographs of serial sections. J Gen Microbiol 13, 327–329.
Blázquez, M.A., Nelson, D.C., and Weijers, D. (2020). Evolution of plant hormone response pathways. Annu Rev Plant Biol 71, 327–353.
Block, M.A., and Jouhet, J. (2015). Lipid trafficking at endoplasmic reticulum-chloroplast membrane contact sites. Curr Opin Cell Biol 35, 21–29.
Bock, D.D., Lee, W.C.A., Kerlin, A.M., Andermann, M.L., Hood, G., Wetzel, A.W., Yurgenson, S., Soucy, E.R., Kim, H.S., and Reid, R.C. (2011). Network anatomy and in vivo physiology of visual cortical neurons. Nature 471, 177–182.
Bon, P., Linarès-Loyez, J., Feyeux, M., Alessandri, K., Lounis, B., Nassoy, P., and Cognet, L. (2018). Self-interference 3D super-resolution microscopy for deep tissue investigations. Nat Methods 15, 449–454.
Bonev, B., and Cavalli, G. (2016). Organization and function of the 3D genome. Nat Rev Genet 17, 661–678.
Boudaoud, A. (2010). An introduction to the mechanics of morphogenesis for plant biologists. Trends Plant Sci 15, 353–360.
Boudière, L., Michaud, M., Petroutsos, D., Rébeillé, F., Falconet, D., Bastien, O., Roy, S., Finazzi, G., Rolland, N., Jouhet, J., et al. (2014). Glycerolipids in photosynthesis: composition, synthesis and trafficking. Biochim Biophys Acta 1837, 470–480.
Brillada, C., and Rojas-Pierce, M. (2017). Vacuolar trafficking and biogenesis: a maturation in the field. Curr Opin Plant Biol 40, 77–81.
Bringmann, M., Li, E., Sampathkumar, A., Kocabek, T., Hauser, M.T., and Persson, S. (2012). POM-POM2/CELLULOSE SYNTHASE INTERACTING1 is essential for the functional association of cellulose synthase and microtubules in Arabidopsis. Plant Cell 24, 163–177.
Brodersen, C.R., Roddy, A.B., Wason, J.W., and McElrone, A.J. (2019). Functional status of xylem through time. Annu Rev Plant Biol 70, 407–433.
Bullmore, E., and Sporns, O. (2009). Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10, 186–198.
Burch-Smith, T.M., Stonebloom, S., Xu, M., and Zambryski, P.C. (2011). Plasmodesmata during development: re-examination of the importance of primary, secondary, and branched plasmodesmata structure versus function. Protoplasma 248, 61–74.
Burr-Hersey, J.E., Mooney, S.J., Bengough, A.G., Mairhofer, S., and Ritz, K. (2017). Developmental morphology of cover crop species exhibit contrasting behaviour to changes in soil bulk density, revealed by X-ray computed tomography. PLoS ONE 12, e0181872.
Bushby, A.J., P’ng, K.M.Y., Young, R.D., Pinali, C., Knupp, C., and Quantock, A.J. (2011). Imaging three-dimensional tissue architectures by focused ion beam scanning electron microscopy. Nat Protoc 6, 845–858.
Cabrera-Bosquet, L., Fournier, C., Brichet, N., Welcker, C., Suard, B., and Tardieu, F. (2016). High-throughput estimation of incident light, light interception and radiation-use efficiency of thousands of plants in a phenotyping platform. New Phytol 212, 269–281.
Cao, C., Yang, Z., Han, L., Jiang, X., and Ji, G. (2015). Study on in situ analysis of cellulose, hemicelluloses and lignin distribution linked to tissue structure of crop stalk internodal transverse section based on FTIR microspectroscopic imaging. Cellulose 22, 139–149.
Carlsson, A.E. (2018). Membrane bending by actin polymerization. Curr Opin Cell Biol 50, 1–7.
Chan, K.X., Phua, S.Y., Crisp, P., McQuinn, R., and Pogson, B.J. (2016). Learning the languages of the chloroplast: retrograde signaling and beyond. Annu Rev Plant Biol 67, 25–53.
Chao, W., Harteneck, B.D., Liddle, J.A., Anderson, E.H., and Attwood, D. T. (2005). Soft X-ray microscopy at a spatial resolution better than 15 nm. Nature 435, 1210–1213.
Chapman, H.N., Fromme, P., Barty, A., White, T.A., Kirian, R.A., Aquila, A., Hunter, M.S., Schulz, J., DePonte, D.P., Weierstall, U., et al. (2011). Femtosecond X-ray protein nanocrystallography. Nature 470, 73–77.
Chen, J., Zhang, Z., Li, L., Chen, B.C., Revyakin, A., Hajj, B., Legant, W., Dahan, M., Lionnet, T., Betzig, E., et al. (2014). Single-molecule dynamics of enhanceosome assembly in embryonic stem cells. Cell 156, 1274–1285.
Chen, K., Li, G.J., Bressan, R.A., Song, C.P., Zhu, J.K., and Zhao, Y. (2020a). Abscisic acid dynamics, signaling, and functions in plants. J Integr Plant Biol 62, 25–54.
Chen, K.E., Chen, H.Y., Tseng, C.S., and Tsay, Y.F. (2020b). Improving nitrogen use efficiency by manipulating nitrate remobilization in plants Nat Plants 6, 1126–1135.
Chimusa, E.R., Dalvie, S., Dandara, C., Wonkam, A., and Mazandu, G.K. (2019). Post genome-wide association analysis: dissecting computational pathway/network-based approaches. Brief Bioinform 20, 690–700.
Choi, W.G., Miller, G., Wallace, I., Harper, J., Mittler, R., and Gilroy, S. (2017). Orchestrating rapid long-distance signaling in plants with Ca2+, ROS and electrical signals. Plant J 90, 698–707.
Clark, N.M., Van den Broeck, L., Guichard, M., Stager, A., Tanner, H.G., Blilou, I., Grossmann, G., Iyer-Pascuzzi, A.S., Maizel, A., Sparks, E.E., et al. (2020). Novel imaging modalities shedding light on plant biology: start small and grow big. Annu Rev Plant Biol 71, 789–816.
Clark, S.E. (1996). Plant cell communication: the world outside the plasma membrane. Trends Plant Sci 1, 406–407.
Cnudde, V., Masschaele, B., Dierick, M., Vlassenbroeck, J., Hoorebeke, L. V., and Jacobs, P. (2006). Recent progress in X-ray CT as a geosciences tool. Appl Geochem 21, 826–832.
Cochard, H., Delzon, S., and Badel, E. (2015). X-ray microtomography (micro-CT): a reference technology for high-resolution quantification of xylem embolism in trees. Plant Cell Environ 38, 201–206.
Cohen, S., Valm, A.M., and Lippincott-Schwartz, J. (2018). Interacting organelles. Curr Opin Cell Biol 53, 84–91.
Conn, A., Pedmale, U.V., Chory, J., and Navlakha, S. (2017). Highresolution laser scanning reveals plant architectures that reflect universal network design principles. Cell Syst 5, 53–62.e3.
Cuevas-Velazquez, C.L., and Dinneny, J.R. (2018). Organization out of disorder: liquid-liquid phase separation in plants. Curr Opin Plant Biol 45, 68–74.
Cui, Y., Li, X., Yu, M., Li, R., Fan, L., Zhu, Y., and Lin, J. (2018a). Sterols regulate endocytic pathways during flg22-induced defense responses in Arabidopsis. Development 145, dev165688.
Cui, Y., Yu, M., Yao, X., Xing, J., Lin, J., and Li, X. (2018b). Single-particle tracking for the quantification of membrane protein dynamics in living plant cells. Mol Plant 11, 1315–1327.
Cui, Y., Cao, W., He, Y., Zhao, Q., Wakazaki, M., Zhuang, X., Gao, J., Zeng, Y., Gao, C., Ding, Y., et al. (2019a). A whole-cell electron tomography model of vacuole biogenesis in Arabidopsis root cells Nat Plants 5, 95–105.
Cui, Y., Zhang, X., Yu, M., Zhu, Y., Xing, J., and Lin, J. (2019b). Techniques for detecting protein-protein interactions in living cells: principles, limitations, and recent progress. Sci China Life Sci 62, 619–632.
Cyranoski, D. (2018). Beijing launches pioneering brain-science centre. Nature 556, 157–158.
Daněk, M., Angelini, J., Malínská, K., Andrejch, J., Amlerová, Z., Kocourková, D., Brouzdová, J., Valentová, O., Martinec, J., and Petrášek, J. (2020). Cell wall contributes to the stability of plasma membrane nanodomain organization of Arabidopsis thaliana FLOTILLIN2 and HYPERSENSITIVE INDUCED REACTION1 proteins. Plant J 101, 619–636.
Dekker, J., and Misteli, T. (2015). Long-range chromatin interactions. Cold Spring Harb Perspect Biol 7, a019356.
Deng, Y., Finck, A., and Fan, R. (2019). Single-cell omics analyses enabled by microchip technologies. Annu Rev Biomed Eng 21, 365–393.
Denk, W., and Horstmann, H. (2004). Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol 2, e329.
Dhondt, S., Vanhaeren, H., Van Loo, D., Cnudde, V., and Inzé, D. (2010). Plant structure visualization by high-resolution X-ray computed tomography. Trends Plant Sci 15, 419–422.
Ding, Y., Wang, J., Wang, J., Stierhof, Y.D., Robinson, D.G., and Jiang, L. (2012). Unconventional protein secretion. Trends Plant Sci 17, 606–615.
Ding, Y., Robinson, D.G., and Jiang, L. (2014). Unconventional protein secretion (UPS) pathways in plants. Curr Opin Cell Biol 29, 107–115.
Dodt, H.U., Leischner, U., Schierloh, A., Jährling, N., Mauch, C.P., Deininger, K., Deussing, J.M., Eder, M., Zieglgänsberger, W., and Becker, K. (2007). Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain. Nat Methods 4, 331–336.
Donohoe, B.S., Kang, B.H., Gerl, M.J., Gergely, Z.R., McMichael, C.M., Bednarek, S.Y., and Staehelin, L.A. (2013). Cis-Golgi cisternal assembly and biosynthetic activation occur sequentially in plants and algae. Traffic 14, 551–567.
Drakakaki, G., and Dandekar, A. (2013). Protein secretion: How many secretory routes does a plant cell have? Plant Sci 203, 74–78.
Dresselhaus, T., and Franklin-Tong, N. (2013). Male-female crosstalk during pollen germination, tube growth and guidance, and double fertilization. Mol Plant 6, 1018–1036.
Du, F., Mo, Y., Israeli, A., Wang, Q., Yifhar, T., Ori, N., and Jiao, Y. (2020). Leaflet initiation and blade expansion are separable in compound leaf development. Plant J 104, 1073–1087.
Duran-Nebreda, S., and Bassel, G.W. (2017). Bridging scales in plant biology using network science. Trends Plant Sci 22, 1001–1003.
Duran-Nebreda, S., and Bassel, G.W. (2019). Plant behaviour in response to the environment: information processing in the solid state. Phil Trans R Soc B 374, 20180370.
Elbaz, Y., and Schuldiner, M. (2011). Staying in touch: the molecular era of organelle contact sites. Trends Biochem Sci 36, 616–623.
Engel, B.D., Schaffer, M., Kuhn Cuellar, L., Villa, E., Plitzko, J.M., and Baumeister, W. (2015). Native architecture of the Chlamydomonas chloroplast revealed by in situ cryo-electron tomography. eLife 4, e04889.
Erguvan, Ö., Louveaux, M., Hamant, O., and Verger, S. (2019). ImageJ SurfCut: a user-friendly pipeline for high-throughput extraction of cell contours from 3D image stacks. BMC Biol 17, 38.
Fan, L., Hao, H., Xue, Y., Zhang, L., Song, K., Ding, Z., Botella, M.A., Wang, H., and Lin, J. (2013). Dynamic analysis of Arabidopsis AP2 σ subunit reveals a key role in clathrin-mediated endocytosis and plant development. Development 140, 3826–3837.
Fan, L., Li, R., Pan, J., Ding, Z., and Lin, J. (2015). Endocytosis and its regulation in plants. Trends Plant Sci 20, 388–397.
Farooque, A.A., Chang, Y.K., Zaman, Q.U., Groulx, D., Schumann, A.W., and Esau, T.J. (2013). Performance evaluation of multiple ground based sensors mounted on a commercial wild blueberry harvester to sense plant height, fruit yield and topographic features in real-time. Comput Electron Agr 91, 135–144.
Feng, W., Kita, D., Peaucelle, A., Cartwright, H.N., Doan, V., Duan, Q., Liu, M.C., Maman, J., Steinhorst, L., Schmitz-Thom, I., et al. (2018). The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. Curr Biol 28, 666–675.e5.
Feraru, E., Feraru, M.I., Kleine-Vehn, J., Martinière, A., Mouille, G., Vanneste, S., Vernhettes, S., Runions, J., and Friml, J. (2011). PIN polarity maintenance by the cell wall in Arabidopsis. Curr Biol 21, 338–343.
Filadi, R., Theurey, P., and Pizzo, P. (2017). The endoplasmic reticulummitochondria coupling in health and disease: Molecules, functions and significance. Cell Calcium 62, 1–15.
Fiorani, F., and Schurr, U. (2013). Future scenarios for plant phenotyping. Annu Rev Plant Biol 64, 267–291.
Fischer, U., Kucukoglu, M., Helariutta, Y., and Bhalerao, R.P. (2019). The dynamics of cambial stem cell activity. Annu Rev Plant Biol 70, 293–319.
Fox, S., Southam, P., Pantin, F., Kennaway, R., Robinson, S., Castorina, G., Sánchez-Corrales, Y.E., Sablowski, R., Chan, J., Grieneisen, V., et al. (2018). Spatiotemporal coordination of cell division and growth during organ morphogenesis. PLoS Biol 16, e2005952.
Franck, C.M., Westermann, J., and Boisson-Dernier, A. (2018). Plant malectin-like receptor kinases: from cell wall integrity to immunity and beyond. Annu Rev Plant Biol 69, 301–328.
Fu, Z., Peng, D., Zhang, M., Xue, F., Zhang, R., He, W., Xu, T., and Xu, P. (2020). mEosEM withstands osmium staining and Epon embedding for super-resolution CLEM. Nat Methods 17, 55–58.
George Ratcliffe, R., Roscher, A., and Shachar-Hill, Y. (2001). Plant NMR spectroscopy. Prog Nucl Magn Reson Spectr 39, 267–300.
Gierlinger, N., Keplinger, T., and Harrington, M. (2012). Imaging of plant cell walls by confocal Raman microscopy. Nat Protoc 7, 1694–1708.
Glancy, B. (2020). Visualizing mitochondrial form and function within the cell. Trends Mol Med 26, 58–70.
Gong, Z., Xiong, L., Shi, H., Yang, S., Herrera-Estrella, L.R., Xu, G., Chao, D.Y., Li, J., Wang, P.Y., Qin, F., et al. (2020). Plant abiotic stress response and nutrient use efficiency. Sci China Life Sci 63, 635–674.
Gosak, M., Markovič, R., Dolenšek, J., Slak Rupnik, M., Marhl, M., Stožer, A., and Perc, M. (2017). Network science of biological systems at different scales: a review. Phys Life Rev 24, 118–135.
Gu, Y., Kaplinsky, N., Bringmann, M., Cobb, A., Carroll, A., Sampathkumar, A., Baskin, T.I., Persson, S., and Somerville, C.R. (2010). Identification of a cellulose synthase-associated protein required for cellulose biosynthesis. Proc Natl Acad Sci USA 107, 12866–12871.
Guan, C., Wu, B., Yu, T., Wang, Q., Krogan, N.T., Liu, X., and Jiao, Y. (2017). Spatial auxin signaling controls leaf flattening in Arabidopsis. Curr Biol 27, 2940–2950.e4.
Guo, Y., Li, D., Zhang, S., Yang, Y., Liu, J.J., Wang, X., Liu, C., Milkie, D. E., Moore, R.P., Tulu, U.S., et al. (2018). Visualizing intracellular organelle and cytoskeletal interactions at nanoscale resolution on millisecond timescales. Cell 175, 1430–1442.e17.
Gustavsson, A.K., Petrov, P.N., Lee, M.Y., Shechtman, Y., and Moerner, W. E. (2018). 3D single-molecule super-resolution microscopy with a tilted light sheet. Nat Commun 9, 123.
Gutierrez, R., Lindeboom, J.J., Paredez, A.R., Emons, A.M.C., and Ehrhardt, D.W. (2009). Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat Cell Biol 11, 797–806.
Hajj, B., Wisniewski, J., El Beheiry, M., Chen, J., Revyakin, A., Wu, C., and Dahan, M. (2014). Whole-cell, multicolor superresolution imaging using volumetric multifocus microscopy. Proc Natl Acad Sci USA 111, 17480–17485.
Hämmerle, M., and Höfle, B. (2016). Direct derivation of maize plant and crop height from low-cost time-of-flight camera measurements. Plant Methods 12, 50.
Hayworth, K.J., Kasthuri, N., Schalek, R., and Lichtman, J.W. (2006). Automating the collection of ultrathin serial sections for large volume TEM reconstructions. Microsc Microanal 12, 86–87.
Helmstaedter, M., Briggman, K.L., Turaga, S.C., Jain, V., Seung, H.S., and Denk, W. (2013). Connectomic reconstruction of the inner plexiform layer in the mouse retina. Nature 500, 168–174.
Hie, B., Peters, J., Nyquist, S.K., Shalek, A.K., Berger, B., and Bryson, B. D. (2020). Computational methods for single-cell RNA sequencing. Annu Rev Biomed Data Sci 3, 339–364.
Hillnhütter, C., Sikora, R.A., Oerke, E.C., and van Dusschoten, D. (2012). Nuclear magnetic resonance: a tool for imaging belowground damage caused by Heterodera schachtii and Rhizoctonia solani on sugar beet. J Exp Bot 63, 319–327.
Holmans, P., Green, E.K., Pahwa, J.S., Ferreira, M.A.R., Purcell, S.M., Sklar, P., Owen, M.J., O’Donovan, M.C., and Craddock, N. (2009). Gene ontology analysis of GWA study data sets provides insights into the biology of bipolar disorder. Am J Hum Genet 85, 13–24.
Horio, T., and Murata, T. (2014). The role of dynamic instability in microtubule organization. Front Plant Sci 5, 511.
House, A., and Balkwill, K. (2017). FIB-SEM enhances the potential taxonomic significance of internal pollen wall structure at the generic level. Flora 236–237, 44–57.
Howe, G.A., Major, I.T., and Koo, A.J. (2018). Modularity in jasmonate signaling for multistress resilience. Annu Rev Plant Biol 69, 387–415.
Hu, Y.S., Zimmerley, M., Li, Y., Watters, R., and Cang, H. (2014). Single-molecule super-resolution light-sheet microscopy. Chemphyschem 15, 577–586.
Hu, Z., Zhou, Q., Zhang, C., Fan, S., Cheng, W., Zhao, Y., Shao, F., Wang, H.W., Sui, S.F., and Chai, J. (2015). Structural and biochemical basis for induced self-propagation of NLRC4. Science 350, 399–404.
Huang, D., Sun, Y., Ma, Z., Ke, M., Cui, Y., Chen, Z., Chen, C., Ji, C., Tran, T.M., Yang, L., et al. (2019). Salicylic acid-mediated plasmodesmal closure via Remorin-dependent lipid organization. Proc Natl Acad Sci USA 116, 21274–21284.
Hughes, N., Askew, K., Scotson, C.P., Williams, K., Sauze, C., Corke, F., Doonan, J.H., and Nibau, C. (2017). Non-destructive, high-content analysis of wheat grain traits using X-ray micro computed tomography. Plant Methods 13, 76.
Ishida, N., Koizumi, M., and Kano, H. (2000). The NMR microscope: a unique and promising tool for plant science. Ann Bot 86, 259–278.
Jackson, M.D.B., Xu, H., Duran-Nebreda, S., Stamm, P., and Bassel, G.W. (2017). Topological analysis of multicellular complexity in the plant hypocotyl. eLife 6, e26023.
Jackson, M.D.B., Duran-Nebreda, S., Kierzkowski, D., Strauss, S., Xu, H., Landrein, B., Hamant, O., Smith, R.S., Johnston, I.G., and Bassel, G.W. (2019). Global topological order emerges through local mechanical control of cell divisions in the Arabidopsis shoot apical meristem. Cell Syst 8, 53–65.e3.
Jain, S., and Parker, R. (2013). The discovery and analysis of P bodies. In: Chan, E., and Fritzler, M., eds. Ten Years of Progress in GW/P Body Research. Advances in Experimental Medicine and Biology. New York: Springer. 23–43.
Jiang, D., Armour, C.R., Hu, C., Mei, M., Tian, C., Sharpton, T.J., and Jiang, Y. (2019). Microbiome multi-omics network analysis: statistical considerations, limitations, and opportunities. Front Genet 10, 995.
Jin, X., Jiang, Z., Zhang, K., Wang, P., Cao, X., Yue, N., Wang, X., Zhang, X., Li, Y., Li, D., et al. (2018). Three-dimensional analysis of chloroplast structures associated with virus infection. Plant Physiol 176, 282–294.
Jung, J.H., Barbosa, A.D., Hutin, S., Kumita, J.R., Gao, M., Derwort, D., Silva, C.S., Lai, X., Pierre, E., Geng, F., et al. (2020). A prion-like domain in ELF3 functions as a thermosensor in Arabidopsis. Nature 585, 256–260.
Kaestner, A., Schneebeli, M., and Graf, F. (2006). Visualizing three-dimensional root networks using computed tomography. Geoderma 136, 459–469.
Kaminuma, E., Yoshizumi, T., Wada, T., Matsui, M., and Toyoda, T. (2008). Quantitative analysis of heterogeneous spatial distribution of Arabidopsis leaf trichomes using micro X-ray computed tomography. Plant J 56, 470–482.
Karahara, I., Yamauchi, D., Uesugi, K., and Mineyuki, Y. (2015). Three-dimensional imaging of plant tissues using X-ray micro-computed tomography. Plant Morphol 27, 21–26.
Kempfer, R., and Pombo, A. (2020). Methods for mapping 3D chromosome architecture. Nat Rev Genet 21, 207–226.
Kierzkowski, D., Nakayama, N., Routier-Kierzkowska, A.L., Weber, A., Bayer, E., Schorderet, M., Reinhardt, D., Kuhlemeier, C., and Smith, R. S. (2012). Elastic domains regulate growth and organogenesis in the plant shoot apical meristem. Science 335, 1096–1099.
Kim, H., Kwon, H., Kim, S., Kim, M.K., Botella, M.A., Yun, H.S., and Kwon, C. (2016). Synaptotagmin 1 negatively controls the two distinct immune secretory pathways to powdery mildew fungi in Arabidopsis. Plant Cell Physiol 57, 1133–1141.
Kise, M., Zhang, Q., and Rovira Más, F. (2005). A stereovision-based crop row detection method for tractor-automated guidance. Biosyst Eng 90, 357–367.
Klose, C., Venezia, F., Hussong, A., Kircher, S., Schäfer, E., and Fleck, C. (2015). Systematic analysis of how phytochrome B dimerization determines its specificity. Nat Plants 1, 1–8.
Knipfer, T., Fei, J., Gambetta, G.A., McElrone, A.J., Shackel, K.A., and Matthews, M.A. (2015). Water transport properties of the grape pedicel during fruit development: insights into xylem anatomy and function using microtomography. Plant Physiol 168, 1590–1602.
Köhler, C., and Springer, N. (2017). Plant epigenomics—Deciphering the mechanisms of epigenetic inheritance and plasticity in plants. Genome Biol 18, 132.
Komis, G., Šamajová, O., Ovečka, M., and Šamaj, J. (2015). Super-resolution microscopy in plant cell imaging. Trends Plant Sci 20, 834–843.
Koppolu, R., and Schnurbusch, T. (2019). Developmental pathways for shaping spike inflorescence architecture in barley and wheat. J Integr Plant Biol 61, 278–295.
Krzic, U., Gunther, S., Saunders, T.E., Streichan, S.J., and Hufnagel, L. (2012). Multiview light-sheet microscope for rapid in toto imaging. Nat Methods 9, 730–733.
Kurusu, T., Kuchitsu, K., Nakano, M., Nakayama, Y., and Iida, H. (2013). Plant mechanosensing and Ca2+ transport. Trends Plant Sci 18, 227–233.
Kwok, R. (2011). Cell biology: The new cell anatomy. Nature 480, 26–28.
Lacombe, B., and Achard, P. (2016). Long-distance transport of phytohormones through the plant vascular system. Curr Opin Plant Biol 34, 1–8.
Lahiri, S., Chao, J.T., Tavassoli, S., Wong, A.K.O., Choudhary, V., Young, B.P., Loewen, C.J.R., and Prinz, W.A. (2014). A conserved endoplasmic reticulum membrane protein complex (EMC) facilitates phospholipid transfer from the ER to mitochondria. PLoS Biol 12, e1001969.
Lamers, J., van der Meer, T., and Testerink, C. (2020). How plants sense and respond to stressful environments. Plant Physiol 182, 1624–1635.
Lashbrooke, J.G., Adato, A., Lotan, O., Alkan, N., Tsimbalist, T., Rechav, K., Fernandez Moreno, J.P., Widemann, E., Grausem, B., Pinot, F., et al. (2015). The tomato MIXTA-Like transcription factor coordinates fruit epidermis conical cell development and cuticular lipid biosynthesis and assembly. Plant Physiol 169, 2553–2571.
Ledford, H. (2018). The lost art of looking at plants. Nature 553, 396–398.
Leergaard, T.B., Hilgetag, C.C., and Sporns, O. (2012). Mapping the connectome: multi-level analysis of brain connectivity. Front Neuroinform 6, 14.
Leroux, O., Leroux, F., Bellefroid, E., Claeys, M., Couvreur, M., Borgonie, G., Van Hoorebeke, L., Masschaele, B., and Viane, R. (2009). A new preparation method to study fresh plant structures with X-ray computed tomography. J Microsc 233, 1–4.
Levy, A., Zheng, J.Y., and Lazarowitz, S.G. (2015). Synaptotagmin SYTA forms ER-plasma membrane junctions that are recruited to plasmodesmata for plant virus movement. Curr Biol 25, 2018–2025.
Li, J., Blanchoin, L., and Staiger, C.J. (2015). Signaling to actin stochastic dynamics. Annu Rev Plant Biol 66, 415–440.
Li, P., Banjade, S., Cheng, H.C., Kim, S., Chen, B., Guo, L., Llaguno, M., Hollingsworth, J.V., King, D.S., Banani, S.F., et al. (2012). Phase transitions in the assembly of multivalent signalling proteins. Nature 483, 336–340.
Li, X., Ji, G., Chen, X., Ding, W., Sun, L., Xu, W., Han, H., and Sun, F. (2017). Large scale three-dimensional reconstruction of an entire Caenorhabditis elegans larva using AutoCUTS-SEM. J Struct Biol 200, 87–96.
Libault, M., Pingault, L., Zogli, P., and Schiefelbein, J. (2017). Plant systems biology at the single-cell level. Trends Plant Sci 22, 949–960.
Liu, L., and Li, J. (2019). Communications between the endoplasmic reticulum and other organelles during abiotic stress response in plants. Front Plant Sci 10, 749.
Liu, J., Li, J., Wang, H., and Yan, J. (2020a). Application of deep learning in genomics. Sci China Life Sci 63, 1860–1878.
Liu, J., Li, M., Zhang, Q., Wei, X., and Huang, X. (2020b). Exploring the molecular basis of heterosis for plant breeding. J Integr Plant Biol 62, 287–298.
Liu, T.L., Upadhyayula, S., Milkie, D.E., Singh, V., Wang, K., Swinburne, I.A., Mosaliganti, K.R., Collins, Z.M., Hiscock, T.W., Shea, J., et al. (2018a). Observing the cell in its native state: Imaging subcellular dynamics in multicellular organisms. Science 360, eaaq1392.
Liu, X., Wang, J., and Sun, L. (2018b). Structure of the hyperosmolalitygated calcium-permeable channel OSCA1.2. Nat Commun 9, 5060.
Long, T.A., Brady, S.M., and Benfey, P.N. (2008). Systems approaches to identifying gene regulatory networks in plants. Annu Rev Cell Dev Biol 24, 81–103.
Louveaux, M., Julien, J.D., Mirabet, V., Boudaoud, A., and Hamant, O. (2016). Cell division plane orientation based on tensile stress in Arabidopsis thaliana. Proc Natl Acad Sci USA 113, E4294–E4303.
Lucas, M., Kenobi, K., von Wangenheim, D., Voss, U., Swarup, K., De Smet, I., Van Damme, D., Lawrence, T., Peret, B., Moscardi, E., et al. (2013a). Lateral root morphogenesis is dependent on the mechanical properties of the overlaying tissues. Proc Natl Acad Sci USA 110, 5229–5234.
Lucas, W.J., Groover, A., Lichtenberger, R., Furuta, K., Yadav, S.R., Helariutta, Y., He, X.Q., Fukuda, H., Kang, J., Brady, S.M., et al. (2013b). The plant vascular system: evolution, development and functions. J Integr Plant Biol 55, 294–388.
Lumba, S., Toh, S., Handfield, L.F., Swan, M., Liu, R., Youn, J.Y., Cutler, S.R., Subramaniam, R., Provart, N., Moses, A., et al. (2014). A mesoscale abscisic acid hormone interactome reveals a dynamic signaling landscape in Arabidopsis. Dev Cell 29, 360–372.
Luo, C., Fernie, A.R., and Yan, J. (2020). Single-cell genomics and epigenomics: technologies and applications in plants. Trends Plant Sci 25, 1030–1040.
Luo, L., He, Y., Zhao, Y., Xu, Q., Wu, J., Ma, H., Guo, H., Bai, L., Zuo, J., Zhou, J.M., et al. (2019). Regulation of mitochondrial NAD pool via NAD+ transporter 2 is essential for matrix NADH homeostasis and ROS production in Arabidopsis. Sci China Life Sci 62, 991–1002.
Lv, X., Jing, Y., Xiao, J., Zhang, Y., Zhu, Y., Julian, R., and Lin, J. (2017). Membrane microdomains and the cytoskeleton constrain AtHIR1 dynamics and facilitate the formation of an AtHIR1-associated immune complex. Plant J 90, 3–16.
Mairhofer, S., Sturrock, C.J., Bennett, M.J., Mooney, S.J., and Pridmore, T. P. (2015). Extracting multiple interacting root systems using X-ray microcomputed tomography. Plant J 84, 1034–1043.
Maizel, A., von Wangenheim, D., Federici, F., Haseloff, J., and Stelzer, E. H.K. (2011). High-resolution live imaging of plant growth in near physiological bright conditions using light sheet fluorescence microscopy. Plant J 68, 377–385.
Man, Y., Zhao, Y., Ye, R., Lin, J., and Jing, Y. (2018). In vivo cytological and chemical analysis of Casparian strips using stimulated Raman scattering microscopy. J Plant Physiol 220, 136–144.
Martin, C.L., and Chun, M. (2016). The BRAIN initiative: building, strengthening, and sustaining. Neuron 92, 570–573.
Martinière, A., Gayral, P., Hawes, C., and Runions, J. (2011). Building bridges: formin1 of Arabidopsis forms a connection between the cell wall and the actin cytoskeleton. Plant J 66, 354–365.
Martinière, A., Lavagi, I., Nageswaran, G., Rolfe, D.J., Maneta-Peyret, L., Luu, D.T., Botchway, S.W., Webb, S.E.D., Mongrand, S., Maurel, C., et al. (2012). Cell wall constrains lateral diffusion of plant plasma-membrane proteins. Proc Natl Acad Sci USA 109, 12805–12810.
McKenna J.F., Tolmie, A.F., and Runions, J. (2014). Across the great divide: the plant cell surface continuum. Curr Opin Plant Biol 22, 132–140.
McKenna, J.F., Rolfe, D.J., Webb, S.E.D., Tolmie, A.F., Botchway, S.W., Martin-Fernandez, M.L., Hawes, C., and Runions, J. (2019). The cell wall regulates dynamics and size of plasma-membrane nanodomains in Arabidopsis. Proc Natl Acad Sci USA 116, 12857–12862.
McWhite, C.D., Papoulas, O., Drew, K., Cox, R.M., June, V., Dong, O.X., Kwon, T., Wan, C., Salmi, M.L., Roux, S.J., et al. (2020). A pan-plant protein complex map reveals deep conservation and novel assemblies. Cell 181, 460–474.e14.
Medina-Puche, L., Tan, H., Dogra, V., Wu, M., Rosas-Diaz, T., Wang, L., Ding, X., Zhang, D., Fu, X., Kim, C., et al. (2020). A defense pathway linking plasma membrane and chloroplasts and co-opted by pathogens. Cell 182, 1109–1124.e25.
Meier, M., Liu, Y., Lay-Pruitt, K.S., Takahashi, H., and von Wirén, N. (2020). Auxin-mediated root branching is determined by the form of available nitrogen. Nat Plants 6, 1136–1145.
Meng, J.G., Liang, L., Jia, P.F., Wang, Y.C., Li, H.J., and Yang, W.C. (2020). Integration of ovular signals and exocytosis of a Ca2+ channel by MLOs in pollen tube guidance. Nat Plants 6, 143–153.
Michaeli, S., Avin-Wittenberg, T., and Galili, G. (2014). Involvement of autophagy in the direct ER to vacuole protein trafficking route in plants. Front Plant Sci 5, 134.
Min, W., Freudiger, C.W., Lu, S., and Xie, X.S. (2011). Coherent nonlinear optical imaging: beyond fluorescence microscopy. Annu Rev Phys Chem 62, 507–530.
Misra, B.B., Assmann, S.M., and Chen, S. (2014). Plant single-cell and single-cell-type metabolomics. Trends Plant Sci 19, 637–646.
Mohamed, A., Monnier, Y., Mao, Z., Lobet, G., Maeght, J.L., Ramel, M., and Stokes, A. (2017). An evaluation of inexpensive methods for root image acquisition when using rhizotrons. Plant Methods 13, 11.
Montenegro-Johnson, T.D., Stamm, P., Strauss, S., Topham, A.T., Tsagris, M., Wood, A.T.A., Smith, R.S., and Bassel, G.W. (2015). Digital single-cell analysis of plant organ development using 3dCellAtlas. Plant Cell 27, 1018–1033.
Motta, A., Berning, M., Boergens, K.M., Staffler, B., Beining, M., Loomba, S., Hennig, P., Wissler, H., and Helmstaedter, M. (2019). Dense connectomic reconstruction in layer 4 of the somatosensory cortex. Science 366, eaay3134.
Motte, H., Vanneste, S., and Beeckman, T. (2019). Molecular and environmental regulation of root development. Annu Rev Plant Biol 70, 465–488.
Mou, Z., He, Y., Dai, Y., Liu, X., and Li, J. (2000). Deficiency in fatty acid synthase leads to premature cell death and dramatic alterations in plant morphology. Plant Cell 12, 405–417.
Movahed, N., Cabanillas, D.G., Wan, J., Vali, H., Laliberté, J.F., and Zheng, H. (2019). Turnip mosaic virus components are released into the extracellular space by vesicles in infected leaves. Plant Physiol 180, 1375–1388.
Mucha, P.J., Richardson, T., Macon, K., Porter, M.A., and Onnela, J.P. (2010). Community structure in time-dependent, multiscale, and multiplex networks. Science 328, 876–878.
Mueller, S.J., and Reski, R. (2015). Mitochondrial dynamics and the ER: the plant perspective. Front Cell Dev Biol 3, 78.
Mulla, D.J. (2013). Twenty five years of remote sensing in precision agriculture: Key advances and remaining knowledge gaps. Biosyst Eng 114, 358–371.
Narayan, K., and Subramaniam, S. (2015). Focused ion beams in biology. Nat Methods 12, 1021–1031.
Nomura, H., Komori, T., Uemura, S., Kanda, Y., Shimotani, K., Nakai, K., Furuichi, T., Takebayashi, K., Sugimoto, T., Sano, S., et al. (2012). Chloroplast-mediated activation of plant immune signalling in Arabidopsis. Nat Commun 3, 926.
Oda, Y., and Hasezawa, S. (2006). Cytoskeletal organization during xylem cell differentiation. J Plant Res 119, 167–177.
Okano, H., Sasaki, E., Yamamori, T., Iriki, A., Shimogori, T., Yamaguchi, Y., Kasai, K., and Miyawaki, A. (2016). Brain/MINDS: a Japanese national brain project for marmoset neuroscience. Neuron 92, 582–590.
Oldroyd, G.E.D., and Leyser, O. (2020). A plant’s diet, surviving in a variable nutrient environment. Science 368, eaba0196.
Otegui, M.S., and Pennington, J.G. (2019). Electron tomography in plant cell biology. Microscopy 68, 69–79.
Ouyang, M., Li, X., Zhang, J., Feng, P., Pu, H., Kong, L., Bai, Z., Rong, L., Xu, X., Chi, W., et al. (2020). Liquid-liquid phase transition drives intra-chloroplast cargo sorting. Cell 180, 1144–1159.e20.
Ouyang, W., Xiao, Q., Li, G., and Li, X. (2021). Technologies for capturing 3D genome architecture in plants. Trends Plant Sci 26, 196–197.
Ovečka M., Vaškebová, L., Komis, G., Luptovčiak, I., Smertenko, A., and Šamaj, J. (2015). Preparation of plants for developmental and cellular imaging by light-sheet microscopy. Nat Protoc 10, 1234–1247.
Ovečka, M., von Wangenheim, D., Tomančák, P., Šamajová, O., Komis, G., and Šamaj, J. (2018). Multiscale imaging of plant development by light-sheet fluorescence microscopy. Nat Plants 4, 639–650.
Paez Valencia, J., Goodman, K., and Otegui, M.S. (2016). Endocytosis and endosomal trafficking in plants. Annu Rev Plant Biol 67, 309–335.
Paredez, A.R., Somerville, C.R., and Ehrhardt, D.W. (2006). Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312, 1491–1495.
Paredez, A.R., Persson, S., Ehrhardt, D.W., and Somerville, C.R. (2008). Genetic evidence that cellulose synthase activity influences microtubule cortical array organization. Plant Physiol 147, 1723–1734.
Pastor-Cantizano, N., Bernat-Silvestre, C., Marcote, M.J., and Aniento, F. (2018). Loss of Arabidopsis p24 function affects ERD2 trafficking and Golgi structure, and activates the unfolded protein response. J Cell Sci 131, jcs203802.
Paterlini, A., Belevich, I., Jokitalo, E., and Helariutta, Y. (2020). Computational tools for serial block electron microscopy reveal plasmodesmata distributions and wall environments. Plant Physiol 184, 53–64.
Perraki, A., Gronnier, J., Gouguet, P., Boudsocq, M., Deroubaix, A.F., Simon, V., German-Retana, S., Legrand, A., Habenstein, B., Zipfel, C., et al. (2018). REM1.3’s phospho-status defines its plasma membrane nanodomain organization and activity in restricting PVX cell-to-cell movement. PLoS Pathog 14, e1007378.
Pérez-Sancho, J., Vanneste, S., Lee, E., McFarlane, H.E., Esteban Del Valle, A., Valpuesta, V., Friml, J., Botella, M.A., and Rosado, A. (2015). The Arabidopsis Synaptotagmin1 is enriched in endoplasmic reticulum-plasma membrane contact sites and confers cellular resistance to mechanical stresses. Plant Physiol 168, 132–143.
Pierret, A., Capowiez, Y., Moran, C.J., and Kretzschmar, A. (1999). X-ray computed tomography to quantify tree rooting spatial distributions. Geoderma 90, 307–326.
Poo, M.M., Du, J.L., Ip, N.Y., Xiong, Z.Q., Xu, B., and Tan, T. (2016). China Brain Project: Basic neuroscience, brain diseases, and brain-inspired computing. Neuron 92, 591–596.
Protter, D.S.W., and Parker, R. (2016). Principles and properties of stress granules. Trends Cell Biol 26, 668–679.
Qi, J., Wu, B., Feng, S., Lü, S., Guan, C., Zhang, X., Qiu, D., Hu, Y., Zhou, Y., Li, C., et al. (2017). Mechanical regulation of organ asymmetry in leaves. Nat Plants 3, 724–733.
Qi, J., Song, C.P., Wang, B., Zhou, J., Kangasjärvi, J., Zhu, J.K., and Gong, Z. (2018). Reactive oxygen species signaling and stomatal movement in plant responses to drought stress and pathogen attack. J Integr Plant Biol 60, 805–826.
Rausenberger, J., Hussong, A., Kircher, S., Kirchenbauer, D., Timmer, J., Nagy, F., Schäfer, E., and Fleck, C. (2010). An integrative model for phytochrome B mediated photomorphogenesis: from protein dynamics to physiology. PLoS ONE 5, e10721.
Reinhardt, D., and Kuhlemeier, C. (2002). Plant architecture. EMBO Rep 3, 846–851.
Rellán-Álvarez, R., Lobet, G., Lindner, H., Pradier, P.L., Sebastian, J., Yee, M.C., Geng, Y., Trontin, C., LaRue, T., Schrager-Lavelle, A., et al. (2015). GLO-Roots: an imaging platform enabling multidimensional characterization of soil-grown root systems. eLife 4, e07597.
Ren, Z., Zhang, Y., Zhang, Y., He, Y., Du, P., Wang, Z., Sun, F., and Ren, H. (2019). Cryo-EM structure of actin filaments from Zea mays pollen Plant Cell 31, 2855–2867.
Rhee, S.Y., Birnbaum, K.D., and Ehrhardt, D.W. (2019). Towards building a plant cell atlas. Trends Plant Sci 24, 303–310.
Rich-Griffin, C., Stechemesser, A., Finch, J., Lucas, E., Ott, S., and Schäfer, P. (2020). Single-cell transcriptomics: a high-resolution avenue for plant functional genomics. Trends Plant Sci 25, 186–197.
Ripoll, J.J., Zhu, M., Brocke, S., Hon, C.T., Yanofsky, M.F., Boudaoud, A., and Roeder, A.H.K. (2019). Growth dynamics of the Arabidopsis fruit is mediated by cell expansion. Proc Natl Acad Sci USA 116, 25333–25342.
Risco, C., de Castro, I.F., Sanz-Sánchez, L., Narayan, K., Grandinetti, G., and Subramaniam, S. (2014). Three-dimensional imaging of viral infections. Annu Rev Virol 1, 453–473.
Rogers, E.D., Monaenkova, D., Mijar, M., Nori, A., Goldman, D.I., and Benfey, P.N. (2016). X-ray computed tomography reveals the response of root system architecture to soil texture. Plant Physiol 171, 2028–2040.
Rokitta, M., Peuke, A.D., Zimmermann, U., and Haase, A. (1999). Dynamic studies of phloem and xylein flow in fully differentiated plants by fast nuclear-magnetic-resonance microimaging. Protoplasma 209, 126–131.
Rosquete, M.R., Worden, N., Ren, G., Sinclair, R.M., Pfleger, S., Salemi, M., Phinney, B.S., Domozych, D., Wilkop, T., and Drakakaki, G. (2019). AtTRAPPC11/ROG2: A role for TRAPPs in maintenance of the plant trans-Golgi network/early endosome organization and function. Plant Cell 31, 1879–1898.
Roussel, J., Geiger, F., Fischbach, A., Jahnke, S., and Scharr, H. (2016). 3D surface reconstruction of plant seeds by volume carving: performance and accuracies. Front Plant Sci 7, 745.
Sablowski, R. (2016). Coordination of plant cell growth and division: collective control or mutual agreement? Curr Opin Plant Biol 34, 54–60.
Saheki, Y., and De Camilli, P. (2017). Endoplasmic reticulum-plasma membrane contact sites. Annu Rev Biochem 86, 659–684.
Sahl, S.J., Hell, S.W., and Jakobs, S. (2017). Fluorescence nanoscopy in cell biology. Nat Rev Mol Cell Biol 18, 685–701.
Samiei, S., Rasti, P., Ly Vu, J., Buitink, J., and Rousseau, D. (2020). Deep learning-based detection of seedling development. Plant Methods 16, 103.
Sampathkumar, A., Gutierrez, R., McFarlane, H.E., Bringmann, M., Lindeboom, J., Emons, A.M., Samuels, L., Ketelaar, T., Ehrhardt, D. W., and Persson, S. (2013). Patterning and lifetime of plasma membrane-localized cellulose synthase is dependent on actin organization in Arabidopsis interphase cells. Plant Physiol 162, 675–688.
Sapala, A., Runions, A., Routier-Kierzkowska, A.L., Das Gupta, M., Hong, L., Hofhuis, H., Verger, S., Mosca, G., Li, C.B., Hay, A., et al. (2018). Why plants make puzzle cells, and how their shape emerges. eLife 7, e32794.
Schalek, R., Kasthuri, N., Hayworth, K., Berger, D., Tapia, J., Morgan, J., Turaga, S., Fagerholm, E., Seung, H., and Lichtman, J. (2011). Development of high-throughput, high-resolution 3D reconstruction of large-volume biological tissue using automated tape collection ultramicrotomy and scanning electron microscopy. Microsc Microanal 17, 966–967.
Schermelleh, L., Ferrand, A., Huser, T., Eggeling, C., Sauer, M., Biehlmaier, O., and Drummen, G.P.C. (2019). Super-resolution microscopy demystified. Nat Cell Biol 21, 72–84.
Schoenaers, S., Balcerowicz, D., Breen, G., Hill, K., Zdanio, M., Mouille, G., Holman, T.J., Oh, J., Wilson, M.H., Nikonorova, N., et al. (2018). The auxin-regulated CrRLK1L kinase ERULUS controls cell wall composition during root hair tip growth. Curr Biol 28, 722–732.e6.
Schulze, A., Zimmer, M., Mielke, S., Stellmach, H., Melnyk, C.W., Hause, B., and Gasperini, D. (2019). Wound-induced shoot-to-root relocation of JA-Ile precursors coordinates Arabidopsis growth. Mol Plant 12, 1383–1394.
Selinski, J., and Scheibe, R. (2019). Malate valves: old shuttles with new perspectives. Plant Biol J 21, 21–30.
Sena, G., Frentz, Z., Birnbaum, K.D., and Leibler, S. (2011). Quantitation of cellular dynamics in growing Arabidopsis roots with light sheet microscopy. PLoS ONE 6, e21303.
Serrano, I., Audran, C., and Rivas, S. (2016). Chloroplasts at work during plant innate immunity. J Exp Bot 67, 3845–3854.
Shen, J., Zhao, Q., Wang, X., Gao, C., Zhu, Y., Zeng, Y., and Jiang, L. (2018). A plant Bro1 domain protein BRAF regulates multivesicular body biogenesis and membrane protein homeostasis. Nat Commun 9, 3784.
Shen, W., Ma, L., Zhang, X., Li, X., Zhao, Y., Jing, Y., Feng, Y., Tan, X., Sun, F., and Lin, J. (2020). Three-dimensional reconstruction of Picea wilsonii Mast. pollen grains using automated electron microscopy. Sci China Life Sci 63, 171–179.
Shi, B., Guo, X., Wang, Y., Xiong, Y., Wang, J., Hayashi, K.I., Lei, J., Zhang, L., and Jiao, Y. (2018). Feedback from lateral organs controls shoot apical meristem growth by modulating auxin transport. Dev Cell 44, 204–216.e6.
Shimada, T., Takagi, J., Ichino, T., Shirakawa, M., and Hara-Nishimura, I. (2018). Plant vacuoles. Annu Rev Plant Biol 69, 123–145.
Siao, W., Wang, P., Voigt, B., Hussey, P.J., and Baluska, F. (2016). Arabidopsis SYT1 maintains stability of cortical endoplasmic reticulum networks and VAP27-1-enriched endoplasmic reticulum-plasma membrane contact sites. J Exp Bot 67, 6161–6171.
Silva, B.S.C., DiGiovanni, L., Kumar, R., Carmichael, R.E., Kim, P.K., and Schrader, M. (2020). Maintaining social contacts: The physiological relevance of organelle interactions. Biochim Biophys Acta 1867, 118800.
Sole, R.V., and Goodwin, B.C. (2002). Signs of Life: How Complexity Pervades Biology. New York: Basic Books.
Somerville, C., Bauer, S., Brininstool, G., Facette, M., Hamann, T., Milne, J., Osborne, E., Paredez, A., Persson, S., Raab, T., et al. (2004). Toward a systems approach to understanding plant cell walls. Science 306, 2206–2211.
Staedler, Y.M., Masson, D., and Schönenberger, J. (2013). Plant tissues in 3D via X-ray tomography: simple contrasting methods allow high resolution imaging. PLoS ONE 8, e75295.
Stefano, G., and Brandizzi, F. (2018). Advances in plant ER architecture and dynamics. Plant Physiol 176, 178–186.
Strauss, M.P., Liew, A.T.F., Turnbull, L., Whitchurch, C.B., Monahan, L. G., and Harry, E.J. (2012). 3D-SIM super resolution microscopy reveals a bead-like arrangement for FtsZ and the division machinery: implications for triggering cytokinesis. PLoS Biol 10, e1001389.
Sturrock, C.J., Woodhall, J., Brown, M., Walker, C., Mooney, S.J., and Ray, R.V. (2015). Effects of damping-off caused by Rhizoctonia solani anastomosis group 2–1 on roots of wheat and oil seed rape quantified using X-ray Computed Tomography and real-time PCR. Front Plant Sci 6, 461.
Sun, J., Zhang, M., Qi, X., Doyle, C., and Zheng, H. (2020). Armadillo-repeat kinesin1 interacts with Arabidopsis atlastin RHD3 to move ER with plus-end of microtubules. Nat Commun 11, 5510.
Takeuchi, H., and Higashiyama, T. (2012). A species-specific cluster of defensin-like genes encodes diffusible pollen tube attractants in Arabidopsis. PLoS Biol 10, e1001449.
Tang, J., and Chu, C. (2017). MicroRNAs in crop improvement: fine-tuners for complex traits. Nat Plants 3, 17077.
Tang, L., Yang, G., Ma, M., Liu, X., Li, B., Xie, J., Fu, Y., Chen, T., Yu, Y., Chen, W., et al. (2020). An effector of a necrotrophic fungal pathogen targets the calcium-sensing receptor in chloroplasts to inhibit host resistance. Mol Plant Pathol 21, 686–701.
Tardieu, F., Cabrera-Bosquet, L., Pridmore, T., and Bennett, M. (2017). Plant phenomics, from sensors to knowledge. Curr Biol 27, R770–R783.
Ten years of Methods. (2014). Nat Methods 11, 1000–1001.
Thapa, S., Zhu, F., Walia, H., Yu, H., and Ge, Y. (2018). A novel LiDAR-based instrument for high-throughput, 3D measurement of morphological traits in maize and sorghum. Sensors 18, 1187.
Thorup-Kristensen, K., Halberg, N., Nicolaisen, M.H., Olesen, J.E., and Dresbøll, D.B. (2020). Exposing deep roots: a rhizobox laboratory. Trends Plant Sci 25, 418–419.
Tilsner, J., Nicolas, W., Rosado, A., and Bayer, E.M. (2016). Staying tight: plasmodesmal membrane contact sites and the control of cell-to-cell connectivity in plants. Annu Rev Plant Biol 67, 337–364.
Titze, B., and Genoud, C. (2016). Volume scanning electron microscopy for imaging biological ultrastructure. Biol Cell 108, 307–323.
Toyota, M., Spencer, D., Sawai-Toyota, S., Jiaqi, W., Zhang, T., Koo, A.J., Howe, G.A., and Gilroy, S. (2018). Glutamate triggers long-distance, calcium-based plant defense signaling. Science 361, 1112–1115.
Tracy, S.R., Roberts, J.A., Black, C.R., McNeill, A., Davidson, R., and Mooney, S.J. (2010). The X-factor: visualizing undisturbed root architecture in soils using X-ray computed tomography. J Exp Bot 61, 311–313.
Tran, L.S.P., Urao, T., Qin, F., Maruyama, K., Kakimoto, T., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2007). Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci USA 104, 20623–20628.
Truskina, J., Han, J., Chrysanthou, E., Galvan-Ampudia, C.S., Lainé, S., Brunoud, G., Macé, J., Bellows, S., Legrand, J., Bågman, A.M., et al. (2021). A network of transcriptional repressors modulates auxin responses. Nature 589, 116–119.
Tsuda, K., Abraham-Juarez, M.J., Maeno, A., Dong, Z., Aromdee, D., Meeley, R., Shiroishi, T., Nonomura, K.I., and Hake, S. (2017). KNOTTED1 cofactors, BLH12 and BLH14, regulate internode patterning and vein anastomosis in maize. Plant Cell 29, 1105–1118.
Uyttewaal, M., Burian, A., Alim, K., Landrein, B., Borowska-Wykręt, D., Dedieu, A., Peaucelle, A., Ludynia, M., Traas, J., Boudaoud, A., et al. (2012). Mechanical stress acts via katanin to amplify differences in growth rate between adjacent cells in Arabidopsis. Cell 149, 439–451.
Vain, T., Crowell, E.F., Timpano, H., Biot, E., Desprez, T., Mansoori, N., Trindade, L.M., Pagant, S., Robert, S., Höfte, H., et al. (2014). The cellulase KORRIGAN is part of the cellulose synthase complex. Plant Physiol 165, 1521–1532.
Van As, H. (2007). Intact plant MRI for the study of cell water relations, membrane permeability, cell-to-cell and long distance water transport. J Exp Bot 58, 743–756.
van Dusschoten, D., Metzner, R., Kochs, J., Postma, J.A., Pflugfelder, D., Bühler, J., Schurr, U., and Jahnke, S. (2016). Quantitative 3D analysis of plant roots growing in soil using magnetic resonance imaging. Plant Physiol 170, 1176–1188.
Van Essen, D.C., Smith, S.M., Barch, D.M., Behrens, T.E.J., Yacoub, E., and Ugurbil, K. (2013). The WU-Minn human connectome project: an overview. NeuroImage 80, 62–79.
Verboven, P., Herremans, E., Borisjuk, L., Helfen, L., Ho, Q.T., Tschiersch, H., Fuchs, J., Nicolaï, B.M., and Rolletschek, H. (2013). Void space inside the developing seed of Brassica napus and the modelling of its function. New Phytol 199, 936–947.
Virlet, N., Sabermanesh, K., Sadeghi-Tehran, P., and Hawkesford, M.J. (2016). Field Scanalyzer: An automated robotic field phenotyping platform for detailed crop monitoring. Funct Plant Biol 44, 143–153.
Voelckel, C., Gruenheit, N., and Lockhart, P. (2017). Evolutionary transcriptomics and proteomics: insight into plant adaptation. Trends Plant Sci 22, 462–471.
von Wangenheim, D., Banda, J., Schmitz, A., Boland, J., Bishopp, A., Maizel, A., Stelzer, E.H.K., and Bennett, M. (2020). Early developmental plasticity of lateral roots in response to asymmetric water availability. Nat Plants 6, 73–77.
Wacker, I., and Schroeder, R.R. (2013). Array tomography. J Microsc 252, 93–99.
Waese, J., Fan, J., Pasha, A., Yu, H., Fucile, G., Shi, R., Cumming, M., Kelley, L.A., Sternberg, M.J., Krishnakumar, V., et al. (2017). ePlant: visualizing and exploring multiple levels of data for hypothesis generation in plant biology. Plant Cell 29, 1806–1821.
Wagner, F.R., Watanabe, R., Schampers, R., Singh, D., Persoon, H., Schaffer, M., Fruhstorfer, P., Plitzko, J., and Villa, E. (2020). Preparing samples from whole cells using focused-ion-beam milling for cryoelectron tomography. Nat Protoc 15, 2041–2070.
Wang, D.Y., Zhang, Q., Liu, Y., Lin, Z.F., Zhang, S.X., Sun, M.X., and Sodmergen, M.X. (2010). The levels of male gametic mitochondrial DNA are highly regulated in angiosperms with regard to mitochondrial inheritance. Plant Cell 22, 2402–2416.
Wang, J.T., and Seydoux, G. (2014). P granules. Curr Biol 24, R637–R638.
Wang, J., and Chai, J. (2020). Structural insights into the plant immune receptors PRRs and NLRs. Plant Physiol 182, 1566–1581.
Wang, L., Li, H., Lv, X., Chen, T., Li, R., Xue, Y., Jiang, J., Jin, B., Baluška, F., Šamaj, J., et al. (2015a). Spatiotemporal dynamics of the BRI1 receptor and its regulation by membrane microdomains in living Arabidopsis cells. Mol Plant 8, 1334–1349.
Wang, X., Li, X., Deng, X., Luu, D.T., Maurel, C., and Lin, J. (2015b). Single-molecule fluorescence imaging to quantify membrane protein dynamics and oligomerization in living plant cells. Nat Protoc 10, 2054–2063.
Wang, L., Wang, B., Yu, H., Guo, H., Lin, T., Kou, L., Wang, A., Shao, N., Ma, H., Xiong, G., et al. (2020a). Transcriptional regulation of strigolactone signalling in Arabidopsis. Nature 583, 277–281.
Wang, L., Xue, Y., Xing, J., Song, K., and Lin, J. (2018a). Exploring the spatiotemporal organization of membrane proteins in living plant cells. Annu Rev Plant Biol 69, 525–551.
Wang, N., and Liu, C. (2019). Implications of liquid-liquid phase separation in plant chromatin organization and transcriptional control. Curr Opin Genet Dev 55, 59–65.
Wang, P., Mugume, Y., and Bassham, D.C. (2018b). New advances in autophagy in plants: regulation, selectivity and function. Semin Cell Dev Biol 80, 113–122.
Wang, P., Richardson, C., Hawkins, T.J., Sparkes, I., Hawes, C., and Hussey, P.J. (2016). Plant VAP27 proteins: domain characterization, intracellular localization and role in plant development. New Phytol 210, 1311–1326.
Wang, P., Hawkins, T.J., Richardson, C., Cummins, I., Deeks, M.J., Sparkes, I., Hawes, C., and Hussey, P.J. (2014). The plant cytoskeleton, NET3C, and VAP27 mediate the link between the plasma membrane and endoplasmic reticulum. Curr Biol 24, 1397–1405.
Wang, P., and Hussey, P.J. (2015). Interactions between plant endomembrane systems and the actin cytoskeleton. Front Plant Sci 6.
Wang, P., Pleskot, R., Zang, J., Winkler, J., Wang, J., Yperman, K., Zhang, T., Wang, K., Gong, J., Guan, Y., et al. (2019). Plant AtEH/Pan1 proteins drive autophagosome formation at ER-PM contact sites with actin and endocytic machinery. Nat Commun 10, 5132.
Wang, Q., Ding, S.L., Li, Y., Royall, J., Feng, D., Lesnar, P., Graddis, N., Naeemi, M., Facer, B., Ho, A., et al. (2020b). The allen mouse brain common coordinate framework: a 3D reference atlas. Cell 181, 936–953.e20.
Wang, Q., Huang, Y., Ren, Z., Zhang, X., Ren, J., Su, J., Zhang, C., Tian, J., Yu, Y., Gao, G.F., et al. (2020c). Transfer cells mediate nitrate uptake to control root nodule symbiosis. Nat Plants 6, 800–808.
Wang, R., He, F., Ning, Y., and Wang, G.L. (2020d). Fine-tuning of RBOH-mediated ROS signaling in plant immunity. Trends Plant Sci 25, 1060–1062.
Wang, X., and Mao, T. (2019). Understanding the functions and mechanisms of plant cytoskeleton in response to environmental signals. Curr Opin Plant Biol 52, 86–96.
Wang, Y., and Li, J. (2008). Molecular basis of plant architecture. Annu Rev Plant Biol 59, 253–279.
Wang, Y., Metoki, A., Smith, D.V., Medaglia, J.D., Zang, Y., Benear, S., Popal, H., Lin, Y., and Olson, I.R. (2020e). Multimodal mapping of the face connectome. Nat Hum Behav 4, 397–411.
Wany, A., Foyer, C.H., and Gupta, K.J. (2018). Nitrate, NO and ROS signaling in stem cell homeostasis. Trends Plant Sci 23, 1041–1044.
Wasson, A.P., Nagel, K.A., Tracy, S., and Watt, M. (2020). Beyond digging: noninvasive root and rhizosphere phenotyping. Trends Plant Sci 25, 119–120.
Waszczak, C., Carmody, M., and Kangasjärvi, J. (2018). Reactive oxygen species in plant signaling. Annu Rev Plant Biol 69, 209–236.
Watanabe, S., Punge, A., Hollopeter, G., Willig, K.I., Hobson, R.J., Davis, M.W., Hell, S.W., and Jorgensen, E.M. (2011). Protein localization in electron micrographs using fluorescence nanoscopy. Nat Methods 8, 80–84.
Watt, M., Fiorani, F., Usadel, B., Rascher, U., Muller, O., and Schurr, U. (2020). Phenotyping: new windows into the plant for breeders. Annu Rev Plant Biol 71, 689–712.
White, J.W., Andrade-Sanchez, P., Gore, M.A., Bronson, K.F., Coffelt, T. A., Conley, M.M., Feldmann, K.A., French, A.N., Heun, J.T., Hunsaker, D.J., et al. (2012). Field-based phenomics for plant genetics research. Field Crops Res 133, 101–112.
Whitewoods, C.D., Gonçalves, B., Cheng, J., Cui, M., Kennaway, R., Lee, K., Bushell, C., Yu, M., Piao, C., and Coen, E. (2020). Evolution of carnivorous traps from planar leaves through simple shifts in gene expression. Science 367, 91–96.
Wolny, A., Cerrone, L., Vijayan, A., Tofanelli, R., Barro, A.V., Louveaux, M., Wenzl, C., Strauss, S., Wilson-Sánchez, D., Lymbouridou, R., et al. (2020). Accurate and versatile 3D segmentation of plant tissues at cellular resolution. eLife 9, e57613.
Wu, H., Jaeger, M., Wang, M., Li, B., and Zhang, B.G. (2011). Three-dimensional distribution of vessels, passage cells and lateral roots along the root axis of winter wheat (Triticum aestivum). Ann Bot 107, 843–853.
Wu, J., Sun, Y., Zhao, Y., Zhang, J., Luo, L., Li, M., Wang, J., Yu, H., Liu, G., Yang, L., et al. (2015). Deficient plastidic fatty acid synthesis triggers cell death by modulating mitochondrial reactive oxygen species. Cell Res 25, 621–633.
Wu, L.G., Hamid, E., Shin, W., and Chiang, H.C. (2014). Exocytosis and endocytosis: modes, functions, and coupling mechanisms. Annu Rev Physiol 76, 301–331.
Wu, M.C., and Lin, X. (2009). Prior biological knowledge-based approaches for the analysis of genome-wide expression profiles using gene sets and pathways. Stat Methods Med Res 18, 577–593.
Wu, Q., Li, Y., Lyu, M., Luo, Y., Shi, H., and Zhong, S. (2020). Touch-induced seedling morphological changes are determined by ethylene-regulated pectin degradation. Sci Adv 6, eabc9294.
Wu, S.W., Kumar, R., Iswanto, A.B.B., and Kim, J.Y. (2018). Callose balancing at plasmodesmata. J Exp Bot 69, 5325–5339.
Wu, Y., Wawrzusin, P., Senseney, J., Fischer, R.S., Christensen, R., Santella, A., York, A.G., Winter, P.W., Waterman, C.M., Bao, Z., et al. (2013). Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy. Nat Biotechnol 31, 1032–1038.
Xiao, T.T., Raygoza, A.A., Pérez, J.C., Kirschner, G., Deng, Y., Atkinson, B., Sturrock, C., Lube, V., Wang, J.Y., Lubineau, G., et al. (2019). Emergent protective organogenesis in Date Palms: a morpho-devodynamic adaptive strategy during early development. Plant Cell 31, 1751–1766.
Xie, D., Chen, M., Niu, J., Wang, L., Li, Y., Fang, X., Li, P., and Qi, Y. (2021). Phase separation of SERRATE drives dicing body assembly and promotes miRNA processing in Arabidopsis. Nat Cell Biol 23, 32–39.
Xing, J., Li, X., Wang, X., Lv, X., Wang, L., Zhang, L., Zhu, Y., Shen, Q., Baluška F., Šamaj, J., et al. (2019). Secretion of phospholipase Dδ functions as a regulatory mechanism in plant innate immunity. Plant Cell 31, 3015–3032.
Yamauchi, D., Tamaoki, D., Hayami, M., Takeuchi, M., Karahara, I., Sato, M., Toyooka, K., Nishioka, H., Terada, Y., Uesugi, K., et al. (2013). Micro-CT observations of the 3D distribution of calcium oxalate crystals in cotyledons during maturation and germination in Lotus miyakojimae seeds. Microscopy 62, 353–361.
Yang, M., Ismayil, A., and Liu, Y. (2020). Autophagy in plant-virus interactions. Annu Rev Virol 7, 403–419.
Yang, W.C., Shi, D.Q., and Chen, Y.H. (2010). Female gametophyte development in flowering plants Annu Rev Plant Biol 61, 89–108
Yang, Y., and Guo, Y. (2018). Unraveling salt stress signaling in plants. J Integr Plant Biol 60, 796–804
Ye, H., Ji, C., Guo, R., and Jiang, L. (2020). Membrane contact sites and organelles interaction in plant autophagy. Front Plant Sci 11, 477.
Yu, A., Xie, Y., Pan, X., Zhang, H., Cao, P., Su, X., Chang, W., and Li, M. (2020a). Photosynthetic phosphoribulokinase structures: enzymatic mechanisms and the redox regulation of the Calvin-Benson-Bassham Cycle. Plant Cell 32, 1556–1573.
Yu, M., Li, R., Cui, Y., Chen, W., Li, B., Zhang, X., Bu, Y., Cao, Y., Xing, J., Jewaria, P.K., et al. (2020b). The RALF1-FERONIA interaction modulates endocytosis to mediate control of root growth in Arabidopsis. Development 147, dev189902.
Zeeshan, H.M.A., Lee, G.H., Kim, H.R., and Chae, H.J. (2016). Endoplasmic reticulum stress and associated ROS. Int J Mol Sci 17, 327.
Zhang, C., and Kovacs, J.M. (2012). The application of small unmanned aerial systems for precision agriculture: a review. Precis Agric 13, 693–712.
Zhang, K., and Liu, Z. (2018). A brief introduction of cryo-EM revolution—the Nobel Prize in Chemistry 2017. Sci China Life Sci 61, 368–370.
Zhang, L., Xing, J., and Lin, J. (2019a). At the intersection of exocytosis and endocytosis in plants. New Phytol 224, 1479–1489.
Zhang, M.X., Zhu, S.S., Xu, Y.C., Guo, Y.L., Yang, W.C., and Li, H.J. (2020a). Transcriptional repression specifies the central cell for double fertilization. Proc Natl Acad Sci USA 117, 6231–6236.
Zhang, T., Zheng, Y., and Cosgrove, D.J. (2016). Spatial organization of cellulose microfibrils and matrix polysaccharides in primary plant cell walls as imaged by multichannel atomic force microscopy. Plant J 85, 179–192
Zhang, X., Cui, Y., Yu, M., and Lin, J. (2019b). Single-molecule techniques for imaging exo-endocytosis coupling in cells Trends Plant Sci 24, 879–880.
Zhang, X., Cui, Y., Yu, M., Su, B., Gong, W., Baluška, F., Komis, G., Šamaj, J., Shan, X., and Lin, J. (2019c). Phosphorylation-mediated dynamics of nitrate transceptor NRT1.1 regulate auxin flux and nitrate signaling in lateral root growth. Plant Physiol 181, 480–498.
Zhang, X., Hu, Z., Guo, Y., Shan, X., Li, X., and Lin, J. (2020b). High-efficiency procedure to characterize, segment, and quantify complex multicellularity in raw micrographs in plants. Plant Methods 16, 100.
Zhang, Y., Li, Z., Chen, N., Huang, Y., and Huang, S. (2020c). Phase separation of Arabidopsis EMB1579 controls transcription, mRNA splicing, and development. PLoS Biol 18, e3000782.
Zhao, F., Du, F., Oliveri, H., Zhou, L., Ali, O., Chen, W., Feng, S., Wang, Q., Lu, S., Long, M., et al. (2020a). Microtubule-mediated wall ani-sotropy contributes to leaf blade flattening. Curr Biol 30, 3972–3985.e3976.
Zhao, J., Zhang, X., Hong, Y., and Liu, Y. (2016). Chloroplast in plant-virus interaction. Front Microbiol 7.
Zhao, P., Zhou, X., Zheng, Y., Ren, Y., and Sun, M.X. (2020b). Equal parental contribution to the transcriptome is not equal control of embryogenesis. Nat Plants 6, 1354–1364.
Zhao, S., Cheng, L., Gao, Y., Zhang, B., Zheng, X., Wang, L., Li, P., Sun, Q., and Li, H. (2019a). Plant HP1 protein ADCP1 links multivalent H3K9 methylation readout to heterochromatin formation. Cell Res 29, 54–66.
Zhao, X., Guo, X., Tang, X., Zhang, H., Wang, M., Kong, Y., Zhang, X., Zhao, Z., Lv, M., and Li, L. (2018a). Misregulation of ER-Golgi vesicle transport induces ER stress and affects seed vigor and stress response. Front Plant Sci 9, 658.
Zhao, Y., Luo, L., Xu, J., Xin, P., Guo, H., Wu, J., Bai, L., Wang, G., Chu, J., Zuo, J., et al. (2018b). Malate transported from chloroplast to mitochondrion triggers production of ROS and PCD in Arabidopsis thaliana. Cell Res 28, 448–461.
Zhao, Y., Man, Y., Wen, J., Guo, Y., and Lin, J. (2019b). Advances in imaging plant cell walls. Trends Plant Sci 24, 867–878.
Zhao, Y., Yu, H., Zhou, J.M., Smith, S.M., and Li, J. (2020c). Malate circulation: Linking chloroplast metabolism to mitochondrial ROS. Trends Plant Sci 25, 446–454.
Zhao, Y.G., and Zhang, H. (2020). Phase separation in membrane biology: the interplay between membrane-bound organelles and membraneless condensates. Dev Cell 55, 30–44.
Zhong, S., and Qu, L.J. (2019a). Cysteine-rich peptides: signals for pollen tube guidance, species isolation and beyond. Sci China Life Sci 62, 1243–1245.
Zhong, S., and Qu, L.J. (2019b). Peptide/receptor-like kinase-mediated signaling involved in male-female interactions. Curr Opin Plant Biol 51, 7–14.
Zhu, M., and Roeder, A.H. (2020). Plants are better engineers: the complexity of plant organ morphogenesis. Curr Opin Genets Dev 63, 16–23.
Zong, W., Zhao, J., Chen, X., Lin, Y., Ren, H., Zhang, Y., Fan, M., Zhou, Z., Cheng, H., Sun, Y., et al. (2015). Large-field high-resolution two-photon digital scanned light-sheet microscopy. Cell Res 25, 254–257.
Acknowledgements
This work was supported by the National Natural Science Foundation of China (31530084, 32000558, 32000483, and 31800504), the Programme of Introducing Talents of Discipline to Universities (111 project, B13007), and the China Postdoctoral Science Foundation Grant (2019M660494).
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Zhang, X., Man, Y., Zhuang, X. et al. Plant multiscale networks: charting plant connectivity by multi-level analysis and imaging techniques. Sci. China Life Sci. 64, 1392–1422 (2021). https://doi.org/10.1007/s11427-020-1910-1
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DOI: https://doi.org/10.1007/s11427-020-1910-1