A rich and bountiful harvest: Key discoveries in plant cell biology

Abstract

The field of plant cell biology has a rich history of discovery, going back to Robert Hooke's discovery of cells themselves. The development of microscopes and preparation techniques has allowed for the visualization of subcellular structures, and the use of protein biochemistry, genetics, and molecular biology has enabled the identification of proteins and mechanisms that regulate key cellular processes. In this review, seven senior plant cell biologists reflect on the development of this research field in the past decades, including the foundational contributions that their teams have made to our rich, current insights into cell biology. Topics covered include signaling and cell morphogenesis, membrane trafficking, cytokinesis, cytoskeletal regulation, and cell wall biology. In addition, these scientists illustrate the pathways to discovery in this exciting research field.

Figure 1

From the pollen tube to a cell surface signaling module with functions in diverse processes. A, Hallmark features in an elongating pollen tube: an apical vesicular zone (red), subapical actin (green/yellow) mesh, and long actin cables. B, Formin-regulated actin assembly. (Left) FORMIN HOMOLOGY PROTEIN1-stimulated assembly. Image shows three contiguous 1 µm optical sections showing bundles of actin (arrowhead) emanating from the cell membrane (top to bottom). (Middle and right) FORMIN HOMOLOGY PROTEIN5-generated subapical actin mesh (arrowheads). The middle panel shows the assembly of a subapical actin mesh in a pollen tube as it emerged from growth arrest to rapid polarized growth; arrowheads, nascent short actin bundles. The right panel highlights an annular configuration of the subapical actin structure (arrows). C and D, Protein pull-down assays showing that pollen hydration (C) and auxin (D) activate RAC/ROPs (upper panels). E, Nuclei of plant cells expressing IAA17-GFP showing rapid formation of nuclear protein bodies (arrow, as an example) in response to auxin. F, The FERONIA–LLG–RALF trimeric signaling module. G, Wild-type, feronia, and llg1 plants showing the impacts of loss of the signaling module on growth and development. H–J, Functions of FER–LLG1–RALF-related signaling modules in reproduction. H, FERONIA-LLG1-RALF controls stigma ROS to regulate pollen germination. I, Pollen tube growth/integrity; image shows that only half the ovules were fertilized (reflected by blue dots) by pollen tubes from a heterozygous male parent (BUPS1/-). J, FERONIA controls multiple steps in pollen–pistil interactions: in wild-type pistils, single pollen tubes exit from the septum (arrows) and enter individual ovules to release sperm for fertilization. In feronia pistils, bundled pollen tubes exit from the septum (arrowheads) and enter into individual ovules; asterisks show pollen tube pile-up from nonruptured pollen tubes in mutant female gametophytes. Scale bars: 10 µm (A and B), 5 µm (E), 3 cm (F), 250 µm (I), and 100 µm (J). A from Cheung and Wu (2004)  Figure 6D; (B) adapted from Cheung and Wu (2004)  Figure 4A and Cheung et al. (2010) Supplemental Figure S5; (C) reprinted from Chen et al. (2013)  Figure 1A, with permission from Elsevier; (D) from Tao et al. (2002)  Figure 5C; (E) from Tao et al. (2005)  Figure 5, A and B; (F) modified from Duan et al. (2010)  Figure 3K and Li et al. (2015)  Figure 11; (G) modified from Li et al. (2015)  Figure 1C; (H) Adapted from Zhang et al., 2021a  Figure 7A; (I) from Ge et al. (2017) Supplemental Figure S6B, reprinted with permission from AAAS; (J) from Duan et al. (2020)  Figure 1B.

Figure 2

Evolution of expansin-related research topics. The figure depicts the development of the expansin research field, starting with the discovery of EXPA as the mediator of acid growth to its involvement in many developmental processes, the discovery of EXPBs with a special function in grass pollination biology, the evolution of expansins as a multigene family, and the discovery of bacterial expansins by way of protein crystallography. Image copyrigth Daniel J. Cosgrove, used with permission.

Figure 3

Endomembrane dynamics of the ER and vacuoles to support a variety of physiological functions. A, Ultrastructure of developing pumpkin seed cells showing PAC vesicles (arrows) responsible for Golgi-independent transport of storage protein precursors to protein storage vacuoles. VSR was discovered from isolated PAC vesicles. VPE converts proproteins to functional mature proteins in the vacuoles. B, GFP-labeled ER network of an A. thaliana cotyledon cell. ER strands rapidly stream along the longitudinal axis of the cell. The ER body is a large ER-derived organelle required for single-cell chemical defense in Brassicaceae plants. C, Endomembrane dynamics responsible for various physiological roles. The ER has the ability to generate distinct compartments with specialized functions. Vacuoles have the ability to remodel their membranes for defense against pathogen infection.

Figure 4

Membrane fusion during cytokinesis (model). A, Membrane vesicles arriving in the plane of cell division contain cis-SNARE complexes on their surfaces. Following disassembly, presumably by the AAA ATPase NSF and its co-factor α-SNAP, the now monomeric Qa-SNARE and R-SNARE proteins are captured by SEC1-related KEULE, which not only prevents reformation of the cis-SNARE complexes but also promotes trans-SNARE complex formation and thus the fusion of vesicles with each other and with the margin of the growing cell plate. Only complexes involving Qa-SNARE KNOLLE (green) and Qbc-SNARE SNAP33 (yellow) are depicted (see B, upper right). B, Evolutionary change of Qa-SNAREs involved in cytokinesis. The ancient SNARE complexes involving Qa-SNARE SYP132 appear conserved throughout the Streptophyta, mediating vesicle fusion during both secretion and cytokinesis. Cytokinesis-specific Qa-SNARE KNOLLE originated by gene duplication with the advent of flowering plants. The encoded protein retained the interaction with the SNARE partners of SYP132, forming two types of cytokinesis-specific SNARE complexes.

Figure 5

MAPs during mitosis. When expressed in tobacco BY-2 cells, GFP-AIR9 labels the PPB (A) but disappears from the cortex at metaphase (B). It reappears in a thin line at the cortex (arrowed in C) when the phragmoplast makes contact. In contrast, GFP-KCBP is detected in the PPB (D) but remains at the cortical division site in a particulate form during metaphase (E) and cytokinesis (F). Scale bar = 20 µm. Reproduced from Buschmann et al. (2015).

Figure 6

Cartoon portraying vesicle-mediated anterograde (COPII vesicles) and retrograde (COPI vesicles) between the ER and Golgi. Vesicle trafficking is accomplished by the sequential operation of long-range tethering complexes (in the case of retrograde trafficking to the ER, the complex includes the plant homolog to TIP20 of the yeast Dsl1 COPI-tethering complex, and in the case of anterograde trafficking to the Golgi, the cis-Golgi tethering complex includes the component p115), and short-range SNARE vesicle fusion complexes. In the case of the ER, this is the cis-SNARE vesicle fusion complex (of which SYP-72 is a component). In this model, ERES and ERIS are in close proximity in a domain of the ER whose size approximates the diameter of an overlying Golgi stack. Golgi stacks are in tight association with the ER via a joint scaffolding matrix of tethering factors. It is proposed that as Golgi stacks move, they capture individual COPII vesicles released from ERES, and simultaneously release COPI vesicles. Both types of vesicles accumulate in the restricted ER–Golgi interface. When the Golgi stacks temporarily stop moving (docking phase), fusion of COPI and COPII vesicles to their respective target membranes takes place. Adapted from Lerich et al. (2012) Figure 13A.

Figure 7

3D tomographic models of a dividing Arabidopsis Golgi stack and TGN cisternae. A, Interactions between the COPII scaffolds (arrowheads) and the cis-side of the Golgi/TGN matrix/scaffold connect ER and Golgi. The dividing Golgi possesses two sets of cis- and medial-cisternae (green, purple, and yellow) held together by the undivided trans-Golgi cisterna (pink). B, Face-on views of the cis-cisternae of the dividing Golgi shown in (A). The C1 and C1′ (orange) and the C2 and C2′ cisternae (green) are cisternal assembly intermediates. COPII vesicles are seen around the margins of these cisternae. C, 3D model images of a Golgi stack with a Golgi-associated TGN (TGN1) and a free, fragmenting TGN (TGN2). C and D, Release of the secretory and CCVs and residual cisternal fragments (asterisk, red) occurs simultaneously.